PhytoKeys 165: 1-25 (2020) A peer-reviewed open-access journal & eo oieene $¢PhytoKeys http:/ / Pp hyto keys -pen soft.net Launched to accelerate biodiversity research lron islands in the Amazon: investigating plant beta diversity of canga outcrops Caroline Oliveira Andrino!?, Rafael Gomes Barbosa-Silva'’, Juliana Lovo!”, Pedro Lage Viana’, Marcelo Freire Moro’, Daniela Cristina Zappi'? | Znstituto Tecnolégico Vale, Belém, Pard, Brazil2. Museu Paraense Emilio Goeldi, Coordenagdo Botanica, Belém, Pard, Brazil3 Instituto de Ciéncias do Mar (Labomar), Universidade Federal do Ceard, Fortaleza, Ceard, Brazil Corresponding author: Caroline Oliveira Andrino (coliveiraandrino@gmail.com) Academic editor: Ricarda Riina | Received 27 May 2020 | Accepted 15 August 2020 | Published 28 October 2020 Citation: Andrino CO, Barbosa-Silva RG, Lovo J, Viana PL, Moro ME, Zappi DC (2020) Iron islands in the Amazon: investigating plant beta diversity of canga outcrops. PhytoKeys 165: 1-25. https://doi.org/10.3897/phytokeys. 165.54819 Abstract The world’s largest mineral iron province, Serra dos Carajas, is home to an open vegetation known as canga, found on top of isolated outcrops rising out of the Amazon rainforest. Over one thousand vascular plants species have been recorded in these canga sites, including 38 edaphic endemics. A new survey adds to our investigation of biogeographic relationships between sixteen canga outcrops and the effect of the distance between site pairs on the number of shared species, regional species turnover and species distribution patterns. Plant collecting expeditions to the westernmost site, the Serra de Campos of Sao Félix do Xingu (SFX), were carried out followed by the identification of all collected specimens and the creation of a species database, built to perform biogeographical analyses. Floristic relationships among the sites were investigated regarding their similarity, using multivariate analyses. The correlation between canga areas and species richness was tested, as well as the geographical distance between pairs of outcrops and their shared species. Vascular plants at SFX total 254 species including 17 edaphic endemics. All canga sites are grouped with 25% of minimum similarity, and the SFX falls within a large subgroup of outcrops. The total species number shared between site pairs does not change significantly with geographical distance but is positively correlated with the area of each outcrop. Meanwhile, shared endemic species numbers between site pairs decline when geographical distance increases, possibly imposed by the barrier of the rainforest. Our data suggest higher shared similarity between the largest and species-richest sites as opposed to geographically nearby sites, and provide useful in- sight for drafting conservation and compensation measures for canga locations. The size of the canga outcrops is associated to higher floristic diversity but connectivity among islands also plays a role in their similarity. Keywords campo rupestre, edaphic endemism, island-like habitats, Neotropical mountains, plant species diversity, rainforest, vascular plant survey Copyright Caroline Oliveira Andrino et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 2 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Introduction Mountaintops are often compared to sky-islands, as their vegetation is often distinct from the surrounding lowlands (Alves and Kolbek 2010; Barres et al. 2019). Montane habitats have been scrutinized due to their high species richness and complexity (Sarki- nen et al. 2012; Antonelli 2015; Kok et al. 2017), arousing scientific interest and have been featured since the first biogeographic studies (Humboldt 1805). In the Amazonian context, open vegetation predominates on exposed rocky surfaces on mountaintops, as opposed to the surrounding lowland rainforest. This vegetation may occur on isolated granite and gneiss inselbergs and quartzitic tepuis, usually above 900 m a.s.l. (Prance 1996; Riina et al. 2019), or over iron-ore conglomerates in the campo rupestre on canga (CRC), found between 600 and 800 ma.s.l. (Viana et al. 2016; Mota et al. 2018; Zappi et al. 2019). ‘There are also island-like lowland ecosystems, such as white sand campinaranas, savannas, and low elevation granitic domes or inselbergs, associated with arenitic and often waterlogged soil in the Amazon region (Gréger and Huber 2007; Adeney et al. 2016; Costa et al. 2019; Henneron et al. 2019; Devecchi et al. 2020). Canga is the lateritic duricrust that covers a supergene iron ore, with poorly de- veloped soil and moderately hard rocks that are very resistant to erosion and perme- able (Gagen et al. 2019). The iron-rich canga presents a series of restrictions to plant establishment, including shallow and rocky soils, high insolation levels, elevated tem- peratures at ground level, extreme water regime — waterlogged soil alternating with up to five months of drought, added to the presence of metals at potentially toxic concen- trations (Schettini et al. 2018). The vegetation in the canga has specific strategies to survive in these stressful edaphic conditions (Gagen et al. 2019), and these conditions have favoured the diversification of edaphic endemic species that are exclusive to the CRC associated with the iron-rich substrate (Giulietti et al. 2019). Species isolation caused by environmental conditions contrasting with the sur- rounding forests and associated with the mosaic of different geomorphological situ- ations in the canga creates also an abundance of micro-habitats (Jacobi et al. 2007; Mota et al. 2015; Silva et al. 2020). It is known that such micro-habitats may be linked to multiple speciation events, and the occurrence of endemism (Bonatelli et al. 2014; Leal et al. 2016; Fiorini et al. 2019; Perrigo et al. 2019; Mota et al. 2020). The first botanical studies on the iron islands of the Serra dos Carajas began in the late 1960s. However, the floristic knowledge was not synthetized and organized until the Flora of the canga of the Serra de Carajas (FCC) project was completed in 2018 (Viana et al. 2016; Mota et al. 2018). This recent flora increased the number of recorded species to 1042 vascular plants (Mota et al. 2018; Salino et al. 2018), and a number of species were confirmed as endemic to the local canga habitat, with 38 species occurring exclusively on this substrate in an area of occupancy of less than 150 km2 (Giulietti et al. 2019). In terms of phytophysiognomies, three major groups were defined by Mota et al. (2015) for Cara- jas: canga vegetation (scrub, bare slab, nodular canga and low forest grove), hydromorphic vegetation (bogs, temporary lagoons, permanent lakes, temporary streams, buriti palm lakes, swampy forest) and other associated forests (mostly at the edge of canga outcrops). Plant beta diversity of canga outcrops 3 Due to historic reasons, collection efforts of the FCC project prioritized some areas of canga, while others still lack in-depth studies. For instance, a research in the canga of the Serra Arqueada (SA) in the municipality of Ourilandia do Norte has recently been completed (Fonseca-da-Silva et al. 2020), while the outcrops located within the recently created Parque Nacional dos Campos Ferruginosos (PNCEF) are still in need of further investigation (Zappi et al. 2019). Giulietti et al. (2019) mentioned the existence of an interesting, isolated area of canga located c. 160 km southwest of the area studied by the FCC known as Serra de Campos, in the municipality of Sao Félix do Xingu (SFX). This study aims to investigate plant distribution and biogeographical patterns that connect the island-like habitats of canga outcrops isolated within an Amazonian rain- forest matrix. We evaluated species distribution in the different sites in order to observe whether canga vegetation has elevated levels of beta diversity and whether the flora of each outcrop will be more dissimilar to other outcrops as the geographical distance in- creases. We provided the first checklist of vascular plants growing on canga at the Serra de Campos of Sao Félix do Xingu (SFX), to add to the dataset we built to investigate the floristic relationship between canga areas, aiming to improve our understanding of the rich and diverse flora of the region. Methods Characterization of the overall study area The CRC are found in the region of Carajas, located in the southeast part the State of Para (Viana et al. 2016; Zappi et al. 2019), one of the largest mineral provinces in the world (Ab’saber 1986). At the Serra dos Carajas, the CRC appears atop a series of out- crops that form discontinuous island-like habitats of open, shrubby or grassy vegetation within a dense matrix of rainforest in the southeastern Amazon basin (Mota et al. 2018). Most of the ferruginous island complex in the southeastern Amazon is within areas protected at different levels. The Serra Norte (SN1, SN2, SN3, SN4, SN5, SN6, SN7, SN8), the Serra Sul (S11A, $11B, $11C S11D) are located in the Floresta Nacional de Carajas, which is an area of sustainable use and thus subject to anthropogenic pres- sures, and iron ore mining currently occurs in areas SN4, SN5 and S11D. The Serra da Bocaina and Serra do Tarzan are the only fully protected areas, and are both inserted within the Parque Nacional dos Campos Ferruginosos (PNCF). However, the Serra Arqueada and Serra de Campos of Sao Félix do Xingu have no legal protection. Floristic list of Serra de Campos The Serra de Campos (SFX) is a canga outcrop found in the municipality of Sao Félix do Xingu, southeastern Para state, Brazilian Amazon. It represents the westernmost limit of the Serra dos Carajas, a complex of ferruginous highland outcrops that extends 4 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) eastwards to the Municipality of Curiondpolis, totalling 126 km2. The plateaus previ- ously studied in the scope of the FCC project (Viana et al. 2016) are found in the Mu- nicipalities of Parauapebas (Serra Norte — SN1 to SN8), and Canaa dos Carajas (Serra Sul — S11, Serra do Tarzan — ST and Serra da Bocaina — SB). The SFX comprises two plateaus measuring c. 9 km2, distant about 1 km from each other, known as SFX1 and SFX2 (Fig. 1). The largest of the two plateaus, known as SFX2, extends for 8.5 km and covers an area of 7.6 km2, while SFX1 is 2.5 km long, measuring 1.4 km2. ‘The pla- teaus are located at 6°23'41"S, 51°52'25"W, with altitudes ranging from 580 to 730 m. a.s.l. (Fig. 1). Distant about 80 km west from SA, the SFX can be accessed through the Municipality of Sao Felix do Xingu first by crossing the Rio Fresco then taking a road that goes through farmland, leading, after a steep climb, to the canga plateaus. Botanical specimens from SFX deposited in herbaria prior to this study were lo- cated through an online search at the Herbarium of the Museu Paraense Emilio Goeldi (MG) and Herbario Ezechias Paulo Heringer (HEPH) (acronyms according to Thiers, continuously updated). Prior to our expeditions, specimens at MG were collected in the 1990’s by Joao Batista Fernandes da Silva and include the type of Mimosa dasilvae A.S.L. Silva & Secco and several gatherings of Orchidaceae, while HEPH currently holds collections made by Annajulia Elizabeth Heringer Salles and J.B.F. Silva in 2001. All materials available in these collections were analyzed and included in this study. Four plant collecting expeditions were carried out between 2016 and 2019 (May 2016, April 2017, March 2018, October 2019), aiming to collect fertile mate- rial of all vascular species. Collecting method followed Filgueiras et al. (1994) with random walks covering the accessible parts of both plateaus, attempting to stop every 1 km to sample the vegetation and collect fertile specimens. We aimed to visit di- verse vegetation types, including open canga slabs, nodular canga, canga scrub, palm swamps (buritizais) and temporary lagoons (Mota et al. 2015) The samples collected were identified to species by comparing their macroscopic and microscopic morphological features with available bibliography, against herbarium collec- tions (physically and on-line) and also consulting key family specialists. Voucher specimens were deposited at MG. Only one collection number per taxon is cited in the present flo- ristic list. A full specimen list is provided in supplement S1. Species names follow Flora do Brasil online (Flora do Brasil under construction), family delimitation followed APG IV (Angiosperm Phylogeny Group 2016) and author abbreviations follow IPNI (2019). Database of the distribution of the flora of Serra dos Carajas Seed plant species distribution data were assembled from the FCC project (Mota et al. 2018), with the compilation of a database comprising 3228 occurrences of 823 species (Zappi et al. 2019). The updates included 23 recent new occurrences for SN1, SN4, SN5, SN7, S11D, and the Serra da Bocaina based on recently collected herbarium material; 149 species for SA (Fonseca-da-Silva et al. 2020); and the newly prepared dataset of SFX. The assembled database comprises 909 seed plant species recorded in CRC at the Carajas Plant beta diversity of canga outcrops 5 51°24'0.000"W 50°54'0.000"W 50°24’0,000"W 49°54'0,000"W 6°0'0.000"S $000°0,009 6°30'0.000"S $«000°0,0E09 wn 2° 3 ha S 2 KR $u000°0,002 51°54'0,000"W 51°24’0,000"W Figure | .a Geographic location of the present study site at SFX and the other study areas from Carajas com- plex b aerial view of an island of canga vegetation surrounding by the rainforest (Photo: Leonardo Vianna) C Serra de Campos of Sao Félix do Xingu (SFX) phytophysiognomy with shrubby and grassy vegetation. complex, including 16 sites (SN1, SN2, SN3, SN4, SN5, SN6, SN7, SN8, S11A, S11B, S11C, S11D, ST, SB, SA and SFX). For the purpose of our analyses, exotic, invasive and weedy species were removed from the dataset as identified in (Giulietti et al. 2018), result- ing in 893 species analysed. The code assigned for each site is found in Table 2. 6 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Biogeographical analyses of the flora of canga sites in the Carajas complex To perform the biogeographical analysis of the CRC of the Carajas complex, the species database was used to investigate the floristic similarity and shared endemicity between different mountaintops across canga sites. Invasive exotic species recorded in each site were excluded from this analysis, as well as specimens with imprecise identification, Lycophytes, and Monilophytes. Floristic similarity between sites was calculated using a presence-absence Matrix (S2, Suppl. material 1) to perform multivariate analysis using ordination and group multivariate methods using the Vegan package in R (Oksanen et al. 2010). We constructed a matrix showing the presence of each species in each site and subjected it to ordination and grouping analyses using a Non-metric Multidimen- sional Scaling (NMDS) and Unweighted Pair Group Method with Arithmetic mean (UPGMA), respectively. Both analyses used Sorensen (Bray-Curtis) index (Legendre and Legendre 2012) to reflect beta diversity between sites. To investigate the floristic richness of sites in relation to the size of each outcrop we used the species count for each canga outcrop and, employing GIS, we calculated the area of each outcrop in square kilometres. A linear model of the recorded richness versus area of each outcrop using the ‘glm’ function with Gaussian model was prepared in R. Because the outcrops were subjected to a large collecting effort during the ‘Flora of Carajas’ Project, we assumed that they were adequately sampled. We also evaluated whether the total number of species and of endemic species shared between sites were significantly related with the geographical distance between them. We computed the centroid of each outcrop using GIS and calculated the geographical distance between the centroids of all outcrop pairs. We tested the normality of the residuals of the mod- els with the Shapiro-Wilk test to see whether the residuals significantly departed from normality. If these did not significantly differ from normality, we accepted the p value of the model. If the residuals differed from normality, we analysed the data using non parametric Spearman’s correlation to evaluate if the correlation was significant. Results Plant species in canga vegetation at Serra de Campos This study recorded a total of 254 species, of which 248 are seed plants, five ferns and one lycophyte in the SFX (Table 1). The richest families recorded are Fabaceae (22 spe- cies), Poaceae (21 spp.), Cyperaceae (15 spp.), Orchidaceae (12 spp.) and Rubiaceae (12 spp.). The five richest genera are Mimosa (Fabaceae), with 5 species, Cyperus and Rhynchospora (Cyperaceae), with 4 species each, and Borreria (Rubiaceae) and Aechmea (Bromeliaceae), with 3 species each. Thirty-seven species are new records for the CRC of the Carajds complex. From these new records, seven belong to the family Orchidaceae, five are new records of Fabaceae, three Annonaceae, and three Sapindaceae. A yet un- described species of Lauraceae was found in SFX, belonging to the genus Dicypellium (Dicypellium aff. caryophyllaceum (Mart.) Nees — PLV 6100, Table 1; Fig. 2). Plant beta diversity of canga outcrops vs ~ AX Figure 2. Representative species of canga in new dataset, SFX a Axonopus longispicus (Doll) Kuhlm b Dicypellium aft. caryophyllaceum (Mart.) Nees € Inga heterophylla Willd d Ipomoea decora Meisn e Matelea microphylla Morillo f Mimosa dasilvae A.S.L. Silva & Secco g Nepsera aquatica (Aubl.) Naudin h Ouratea cearensis (Tiegh.) Sastre & Offroy i Pachyptera incarnata (Aubl.) Francisco & L.G. Lohmann j Passifora picturata Ker Gawl. k Phyllanthus minutulus Mull Arg. | Rodriguezia lanceolata Ruiz & Pav. 8 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Table |. Vascular plant species from Serra de Campos of Sao Félix do Xingu (SFX), discriminated by noy- elties for Flora of the canga of Carajas according to Mota et al. (2018) and Fonseca-da-Silva et al. (2020) endemism in canga outcrops according to Giulietti et al. (2019); endemism in Serra de Campos, and life form and voucher information for each species. Collectors: AHS: Anajulia Heringer Salles; BF: Bruno Fernandes Falcao; COA: Caroline Oliveira Andrino; DCZ: Daniela Cristina Zappi; JBFS: Joao Batista da Silva; MN: Matheus Nogueira; MP: Mayara Pastore; PLV: Pedro Lage Viana. *Invasive exotic species. Taxa New for Endemic Endemic Life form Voucher Carajas Flora _canga SFX Lycophyte Selaginellaceae Selaginella radiata (Aubl.) Spring. Herb DCZ 4055 Monilophytes Dennstaedtiaceae Pteridium arachnoideum (Kauf.) Maxon Herb DCZ 4002 Polypodiaceae Microgramma persicariifolia (Schrad.) C.Presl Herb DCZ 4066 Pleopeltis polypodioides (L.) Andrews & Windham Herb DCZ 3922 Serpocaulon triseriale (Sw.) A.R.Sm. Herb DCZ 4037 Pteridaceae Doryopteris collina (Raddi) J.Sm. Herb DCZ 4040 Spermathophytes Acanthaceae Justicia birae A.S.Reis, F.A.Silva, A.Gil & Kameyama Herb MP 600 Alismataceae Helanthium tenellum (Mart. ex Schult & Schult.f.) Britton Herb MP 613 Limnocharis flava (L.) Buchenau x Herb PLV 6149 Anacardiaceae Anacardium occidentale L. Treelet DCZ 3923 Spondias mombin L. X Treelet DCZ3921 Annonaceae Annona sericea Dunal Xx Shrub DCZ 4051 Annona exsucca DC. Tree COA 658 Guatteria procera R.E.Fr. Xx Tree DCZ 4050 Xylopia aromatica (Lam.) Mart. Treelet DCZ 3970 Apocynaceae Himatanthus cf. articulatus (Vahl) Woodson Tree COA 676 Mandevilla scabra (Hoffmanns. ex Roem. & Schult.) K. Liana DCZ 3880 Schum. Mandevilla tenuifolia (J.C. Mikan) Woodson Herb DCZ 3885 Matelea microphylla Morillo Xx Herb DCZ 3942 Tabernaemontana flavicans Willd. ex Roem. & Schult. Treelet COA 613 Tabernaemontana macrocalyx Mill. Arg. Treelet COA 605 Araceae Anthurium gracile (Rudge) Lindl. Herb DCZ 5017 Anthurium sp.1 Xx Herb DCZ 3898 Arecaceae Mauritia flexuosa Matt. Palm DCZ 3961 Mauritiella armata (Mart.) Burret Palm DCZ 3960 Oenocarpus distichus Mart. Palm DCZ 3948 Syagrus cocoides Matt. Palm DCZ 3892 Asteraceae Emilia fosbergii Nicolson Herb DCZ 4046 Ichthyothere terminalis (Spreng.) S.F. Blake Shrub DCZ 3868 Monogereion carajensis G.M. Barroso & R.M. King Xx Herb DCZ 3861 Riencourtia pedunculosa (Rich.) Pruski Herb DCZ 3924 Tilesia baccata (L.f.) Pruski Herb DCZ 3980 Unxia camphorata Lf. Herb DCZ 3941 Begoniaceae Begonia humilis Dryand Herb DCZ 3973 Plant beta diversity of canga outcrops Taxa Bignoniaceae Adenocalymma schomburgkii (DC.) L.G.Lohmann Amphilophium mansoanum (DC.) L.G.Lohmann Anemopaegma carajasense A.H. Gentry ex Firetti-Leggieri & L.G. Lohmann Anemopaegma longipetiolatum Sprague Jacaranda ulei Bureau & K.Schum. Pachyptera incarnata (Aubl.) Francisco & L.G. Lohmann Pleonotoma melioides (S.Moore) A.H.Gentry Pleonotoma orientalis Sandwith Bixaceae Cochlospermum orinocense (Kunth) Steud. Boraginaceae Cordia nodosa Lam. Bromeliaceae Aechmea castelnavii Baker Aechmea mertensii (G.Mey.) Schult. & Schult.f. Aechmea tocantina Baker Ananas ananassoides (Baker) L.B. Sm. Dyckia duckei L.B.Sm. Tillandsia adpressiflora Mez Burmanniaceae Burmannia capitata (Walter ex J.RGmel.) Mart. Burmannia flava Matt. Cabombaceae Cabomba furcata Schult. & Schult.f. Commelinaceae Commelina erecta L. Dichorisandra hexandra (Aubl.) C.B. Clarke Connaraceae Rourea ligulata Baker Convolvulaceae Distimake macrocalyx (Ruiz & Pav.) A.R. Sim6es & Staples Ipomoea decora Meisn. Ipomoea marabaensis D.F.Austin & Secco Ipomoea rubens Choisy Cucurbitaceae Gurania sinuata (Benth.) Cogn. Cyperaceae Bulbostylis conifera (Kunth) C.B. Clarke Cyperus ageregatus (Willd.) Endl. Cyperus laxus Lam. Cyperus sesquiflorus (Torr.) Mattf. & Kiik. Cyperus sphacelatus Rottb. Diplasia karatifolia Rich. in Pers. Eleocharis flavescens (Poir.) Urb. Eleocharis pedrovianae C.S. Nunes, R. Trevis. & A. Gil Eleocharis plicarhachis (Griseb.) Svenson Rhynchospora barbata (Vahl) Kunth Rhynchospora filiformis Vahl Rhynchospora holoschoenoides (Rich.) Herter Rhynchospora seccoi C.S.Nunes, PJ.S. Silva Filho & A.Gil Scleria cyperina Willd. ex Kunth Scleria microcarpa Nees ex Kunth Dioscoreaceae Dioscorea piperifolia Humb. & Bonpl. ex Willd. Dioscorea trilinguis Griseb. Eriocaulaceae Eriocaulon carajense Moldenke New for Carajas Flora Endemic canga Endemic SFX. Life form Liana Liana Shrub Liana Shrub Liana Liana Liana Treelet Tree Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Liana Shrub Liana Liana Liana Liana Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Liana Liana Herb Voucher COA 611 DCZ 4025 DCZ 3914 DCZ 3867 DCZ 3945 DCZ 4061 COA 638 DCZ 3883 DCZ 3875 COA 641 COA 670 COA 673 AHS 2194 DCZ 3891 DCZ 3872 DCZ 4034 MP 644 DCZ 3903 DCZ 3963 DCZ 4058 DCZ 3858 COA 666 MP 660 DCZ 4057 DCZ 3873 MP 672 AHS 2167 COA 624 DCZ 3865 DCZ 3957 DCZ 4031 DCZ 4042 DCZ 4032 MP 627 DCZ 4027 COA 678 COA 657 DCZ 3930 MP 608 DCZ 3905 DCZ 3925 COA 650 DCZ 3884 DCZ 3934 DCZ 3936 10 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Taxa New for Endemic Endemic Life form Voucher Carajas Flora _canga SFX Eriocaulon cinereum R.Br. Herb DCZ 4049 Paepalanthus fasciculoides Hensold Herb DCZ 3878 Syngonanthus discretifolius (Moldenke) M.T.C. Watanabe Xx Herb PLV 6119 Syngonanthus heteropeplus (Kérn.) Ruhland Herb MP 659 Erythroxylaceae Erythroxylum nelson-rosae Plowman X Shrub COA 672 Erythroxylum rufum Cav. Shrub COA 637 Euphorbiaceae Alchornea discolor Poeppig Shrub DCZ 3886 Aparisthmium cordatum (A. Juss.) Baill. Tree DCZ 3997 Astraea lobata (L.) Klotzsch Shrub DCZ 3955 Mabea angustifolia Spruce ex Benth. Shrub DCZ 3987 Manihot quinquepartita Huber ex D.J.Rogers Shrub DCZ 3954 Manihot tristis Mill.Arg. Shrub MP 666 Maprounea brasiliensis A.St.-Hil. X Shrub DCZ 3991 Fabaceae Abrus melanospermus Hassk. Liana DCZ 3912 Aeschynomene sensistiva var. hispidula (Kunth) Rudd Subshrub =DCZ 4024 Bauhinia pulchella Benth. Shrub DCZ 3869 Camptosema ellipticum (Desv.) Burkart Shrub DCZ 3907 Centrosema carajasense Cavalcante Herb/Liana DCZ 4007 Chamaecrista desvauxii (Collad.) Killip Subshrub DCZ 3946 Clitoria falcata Lam. Liana DCZ 3917 Crotalaria maypurensis Kunth Shrub DCZ 3881 Dioclea apurensis Kunth Liana DCZ 3919 Inga calantha Ducke X Tree COA 600 Inga heterophylla Willd xX Tree DCZ 4036 Inga leiocalycina Benth. Xx Tree MP 598 Mimosa dasilvae A.S.L. Silva & Secco X Xx X Subshrub COA 622 Mimosa guilandinae vat. spruceana (Benth.) Barneby Shrub COA 668 Mimosa skinneri Benth. var. carajarum Barneby X Herb DCZ 3860 Mimosa somnians Humb. & Bonpl. ex Willd. Subshrub =_DCZ 3876 Mimosa xanthocentra Matt. Tree PLV 6158 Parkia platycephala Benth. Shrub DCZ 4013 Periandra mediterranea (Vell.) Taub. Shrub DCZ 3902 Senegalia multipinnata (Ducke) Seigler & Ebinger Treelet COA 603 Stylosanthes capitata Vogel Subshrub ==.DCZ 3977 Tachigali vulgaris L.LG.Silva & H.C.Lima Tree COA 655 Gentianaceae Schultesia benthamiana Klotzsch ex Griseb. Herb DCZ 3928 Heliconiaceae Heliconia psittacorum L.F. xX Herb MP 671 Hypericaceae Vismia gracilis Hieron Treelet COA 654 Iridaceae Cipura xanthomelas Maxim. ex Klatt Herb DCZ 3899 Lamiaceae Amasonia lasiocaulos Mart. & Schau ex Schau. Subshrub =_DCZ 3947 Hyptis atrorubens Poit. Herb DCZ 3981 Mesosphaerum pectinatum (L.) Kuntze Herb MN 697 Mesosphaerum suaveolens (L.) Kuntze Herb DCZ 4048 Vitex panshiniana Moldenke Xx Tree DCZ 4053 Lauraceae Cassytha filiformis L. Parasite DCZ 3874 Dicypellium aff. caryophyllaceum (Mart.) Nees Xx Xx Shrub PLV 6100 Mezilaurus itauba (Meisn.) Taub. ex Mez Shrub DCZ 4001 Rhodostemonodaphne praeclara (Sandwith) Madrifidn x Tree DCZ 3983 Plant beta diversity of canga outcrops Taxa Lentibulariaceae Utricularia neottioides A.St-Hil & Girard Utricularia pusilla Vahl Utricularia subulata L. Loranthaceae Passovia pedunculata (Jacq.) Kuijt Psittacanthus eucalyptifolius (Kunth) G. Don Lythraceae Cuphea annulata Koehne Cuphea carajasensis Loutteig Malpighiaceae Banisteriopsis malifolia (Nees & Mart.) B.Gates Banisteriopsis stellaris (Griseb.) B.Gates Byrsonima chrysophylla Kunth Heteropterys nervosa A.Juss. Malvaceae Waltheria indica L. Marantaceae Monotagma plurispicatum (K6rn.) K.Schum. Marcgraviaceae Norantea guianensis Aubl. Melastomataceae Bellucia grossularioides (L.) Triana Brasilianthus carajensis Almeda & Michelangeli Clidemia capitellata (Bonpl.) D.Don Miconia alternans Naudin Miconia heliotropoides Triana Nepsera aquatica (Aubl.) Naudin Pleroma carajasense K.Rocha, R.Goldenb. & ES.Mey Pterolepis trichotoma (Rottb.) Cogn. Tibouchina edmundboi Brade Menispermaceae Abuta grandifolia (Mart.) Sandwith Cissampelos andromorpha DC. . Metteniusaceae Emmotum nitens (Benth.) Miers Myrtaceae Eugenia punicifolia (Kunth) DC. Myrcia cuprea (O.Berg.) Kiaersk. Myrcia splendens (Sw.) DC. Myrciaria floribunda (H.West ex Willd.) O.Berg Myrciaria glomerata O.Berg Ochnaceae Ouratea castaneifolia (DC.) Engl. Ouratea cearensis (Tiegh.) Sastre & Offroy Ouratea racemiformis Ule Onagraceae Ludwigia cf. latifolia (Benth.) H.Hara Ludwigia nervosa (Poir.) H.Hara Orchidaceae Catasetum boyi Mansf. Catasetum discolor (Lindl.) Lindl. Cyrtopodium andersonii (Lamb. ex Andrews) R.Br. Encyclia chloroleuca (Hook.) Neum. Epidendrum strobiliferum Rchb.f. Erycina pusilla (L.) N.H. Williams & M.W.Chase Habenaria nuda Lindl New for Carajas Flora Endemic canga Endemic SFX. Life form Herb Herb Herb Parasite Parasite Subshrub Shrub Shrub Liana Shrub Liana Shrub Herb Shrub Shrub Herb Shrub Shrub Shrub Herb Shrub Herb Shrub Shrub Liana Shrub Shrub Shrub Shrub Shrub Shrub Treelet Shrub Shrub Subshrub Shrub Herb Herb Herb Herb Herb Herb Herb 11 Voucher MP 664 DCZ 3904 PLV 6139 DCZ 3909 DCZ 4056 DCZ 3864 COA 616 MN 743 DCZ 3863 DCZ 3929 COA 645 DCZ 4064 DCZ 4000 DCZ 3887 DCZ 3995 DCZ 3877 DCZ 4020 DCZ 4021 DCZ 4008 COA 649 DCZ 3910 DCZ 4019 DCZ 3932 COA 646 COA 663 MP 601 DCZ 3894 COA 639 DCZ 3965 DCZ 3915 DCZ 4010 DCZ 3920 COA 604 DCZ 4033 DCZ 3967 COA 674 JBES 648 DCZ 4030 COA 643 JBFS 540 COA 667 JBFS 498 MP 609 12 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Taxa Habenaria orchiocalcar Hoehne Polystachya concreta (Jacq.) Garay & H.R.Sweet Rodriguezia lanceolata Ruiz & Pav. Scaphyglottis cf. livida Sobralia liliastrum Salzm. ex Lindl. Orobanchaceae Buchnera carajasensis Scatigna & N.Mota Passifloraceae Passiflora ceratocarpa F. Silveira Passiflora picturata Ker Gawl. Passiflora tholozanii Sacco Phyllanthaceae Phyllanthus hyssopifolioides Kunth. Phyllanthus minutulus Mill.Arg. Phytolaccaceae Phytolacca thyrsiflora Fenzl ex J. Schmidt Piperaceae Peperomia albopilosa D. Monteiro Peperomia magnoliifolia (Jacq.) A.Diete. Plantaginaceae Scoparia dulcis L. Poaceae Acroceras zizanioides (Kunth) Dandy Andropogon bicornis L. Axonopus cf. longispicus (Doll) Kuhlm. Axonopus rupestris Davidse Eleusine indica (L.) Gaertn.* Hildaea parvispiculata C. Silva & R.P. Oliveira Ichnanthus calvescens (Nees ex Trin.) Doll Luziola peruviana Juss. ex J.F.Gmel. Melinis minutiflora P.Beauv.* Mesosetum cayennense Steud. Oryza glumaepatula Steud. Paspalum axillare Swallen Paspalum foliiforme S.Denham Paspalum reticulinerve Renvoize Rhytachne gonzalezii Davidse Rugoloa pilosa (Sw.) Zuloaga Steinchisma laxum (Sw.) Zuloaga Taquara micrantha (Kunth) 1.L.C.Oliveira & R.P.Oliveira Trachypogon spicatus (L.f.) Kuntze Trichanthecium cf. arctum (Swallen) Zuloaga & Morrone Urochloa maxima (Jacq.) R.D. Webster* Polygalaceae Bredemeyera divaricata (DC.) J.EB. Pastore Caamembeca spectabilis (DC.) J.EB. Pastore Polygala adenophora DC. Portulacaceae Portulaca sedifolia N.E.Br. Primulaceae Cybianthus detergens Mart. Proteaceae Roupala montana Aubl. Rhamnaceae Gouania pyrifolia Reissek Rubiaceae Alibertia edulis (Rich.) A. Rich. ex DC. New for Carajas Flora x xX Endemic canga Endemic SFX. Life form Herb Herb Herb Herb Herb Herb Liana Liana Liana Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Herb Shrub Subshrub Herb Herb Shrub Shrub Liana Shrub Voucher JBES 219 COA 669 COA 665 COA 671 DCZ 3888 DCZ 3931 DCZ 4060 DCZ 3976 COA 612 DCZ 4028 DCZ 4026 DCZ 4041 PLV 6169 COA 647 DCZ 4065 DCZ 4022 DCZ 3950 DCZ 4023 DCZ 3896 DCZ 4045 PLV 6124 DCZ 4011 DCZ 3918 COA 640 PLV 6117 BFF 634 PLV 6130 DCZ 3916 PLV 6166 PLV 6127 DCZ 3964 COA 677 DCZ 3999 DCZ 3944 DCZ 3913 DCZ 3951 DCZ 3911 COA 642 DCZ 3900 DCZ 3862 DCZ 4062 DCZ 4063 DCZ 3953 DCZ 4035 Plant beta diversity of canga outcrops 13 Taxa New for Endemic Endemic Life form Voucher Carajas Flora _canga SFX Borreria alata (Aubl.) DC. Herb DCZ 3866 Borreria carajasensis E.L. Cabral & L.M. Miguel Xx Subshrub =.DCZ 3859 Borreria semiamplexicaulis E.L.Cabral Herb DCZ 3938 Cordiera myrciifolia (K.Schum.) C.H.Perss. & Delprete Shrub DCZ 3971 Coutarea hexandra (Jacq.) K.Schum. X Shrub COA 610 Guettarda argentea Lam. Shrub COA 602 Palicourea guianensis Aubl. Treelet DCZ 4052 Perama carajensis J.H. Kirkbr. Xx Herb DCZ 3879 Psychotria colorata (Willd. ex Schult.) Mull. Arg. Herb DCZ 4017 Psychotria hoffmannseggiana (Willd. ex Schult.) Mull. Arg. Subshrub COA 601 Sabicea grisea Cham. & Schltdl. Liana DCZ 3901 Rutaceae Dictyoloma vandellianum A. Juss. Treelet DCZ 3975 Ertela trifolia (L.) Kuntze Subshrub COA 607 Pilocarpus microphyllus Stapf ex Wardlew. Shrub COA 653 Salicaceae Casearia arborea (Rich.) Urb. Tree DCZ 3982 Casearia javitensis Kunth Shrub DCZ 4014 Sapindaceae Allophylus semidentatus (Migq.) Radlk. Xx Shrub DCZ 3959 Paullinia stellata Radlk. Xx Liana DCZ 4044 Pseudima frutescens (Aubl.) Radlk. Xx Shrub PLV 6151 Serjania lethalis A.St.-Hil. Liana DCZ 3996 Sapotaceae Pouteria ramiflora (Mart.) Radlk. Treelet DCZ 3969 Simaroubaceae Simaba guianensis Aubl. Shrub DCZ 3984 Simarouba amara Aubl. Shrub DCZ 3985 Siparunaceae Siparuna ficoides S.S.Rener & Hausner Treelet COA 660 Smilacaceae Smilax irrorata Matt. ex Griseb Liana DCZ 3935 Solanaceae Solanum americanum Mill. Herb DCZ 4059 Solanum crinitum Lam. Treelet COA 623 Trigoniaceae Trigonia nivea Cambess. Liana COA 651 Turneraceae Turnera glaziovii Urb Shrub DCZ 4012 Turnera laciniata Arbo Herb DCZ 3993 Turnera melochioides Cambess. Shrub PLV 6160 Urticaceae Cecropia palmata Willd. Tree COA 664 Velloziaceae Vellozia glauca Pohl Herb DCZ 3890 Verbenaceae Lantana trifolia L. Xx Shrub MN 755 Lippia grata Schauer Shrub DCZ 3871 Stachytarpheta cayennensis (Rich.) Vahl Subshrub COA 608 Vitaceae Cissus erosa Rich. Liana DCZ 3882 Vochysiaceae Qualea parviflora Matt. Tree MP 624 Xyridaceae Xyris brachysepala Kral xX Herb PLV 6125 SPECIES TOTAL (254) 36 17 2 14 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Table 2. Areas compared by this study, respective area codes used in the multivariate analysis and number of angiosperms species recorded for each area. Serra de Campos of Sao Félix do Xingu (SFX) data is pro- duced by this study, ARQ-CAN data is available in Fonseca-da-Silva et al. (2020) and Flora of the canga of the Serra de Carajas (FCC) data is available in Mota et al. (2018). Area code Area Species Cumulative species ARQ Serra Arqueada 149 149 S11A Serra dos Carajas — Serra Sul 11A 230 535 S11B Serra dos Carajas — Serra Sul 11B 201 SiC Serra dos Carajas — Serra Sul 11C 180 S11D Serra dos Carajas — Serra Sul 11D 428 SN1 Serra dos Carajas — Serra Norte 1 383 643 SN2 Serra dos Carajas — Serra Norte 2 125 SN3 Serra dos Carajas — Serra Norte 3 218 SN4 Serra dos Carajas — Serra Norte 4 308 SN5 Serra dos Carajas — Serra Norte 5 293 SNG Serra dos Carajas — Serra Norte 6 99 SN7 Serra dos Carajas — Serra Norte 7 112 SN8 Serra dos Carajas — Serra Norte 8 101 SB Serra dos Carajas — Serra da Bocaina 223 336 SE Serra dos Carajas — Serra do Tarzan pabl SFX Serra de Campos — Sao Félix do Xingu 248 248 Among the 38 edaphic endemic species of canga, defined according to Giulietti et al. (2019), 17 (c. 50%) were recorded in SFX. Two of these, Erythroxylum nelson-rosae Plow- man (Erythroxylaceae) and Matelea microphylla Morillo (Apocynaceae) were not previous- ly recorded for SFX in the list of endemic edaphic species of the canga of Carajas (Giulietti et al. 2019). One species, Mimosa dasilvae (Fabaceae), is only known to occur in SFX. Around 25% (60) of the 248 angiosperms registered for SFX are restricted to the Amazonian Rainforest biome, but the majority of the flora is widely distributed in open habitats throughout South America. The vegetation of the Serra de Campos Regarding the phytophysiognomies listed by Mota et al. (2015) for the region, the canga vegetation of the SFX has a predominance of vast spreads of scrub composed of closely disposed treelets and shrubs. Amongst them, treelets and shrubs such as Byrsonima chrysophylla Kunth, Cordiera myrciifolia (K.Schum.) C.H.Perss. & Delprete, Anemopaegma carajasense A.H. Gentry ex Firetti-Leggieri & L.G. Lohmann*, Cuphea annulata Koehne, Lippia grata Schauer, Erythroxylum nelson-rosae Plowman™, Syagrus cocoides Matt., as well as several species of Myrcia and Eugenia, the palm Syagrus cocoides Mart. and scramblers and climbers such as Norantea guianensis Aubl., Cissus erosa Rich., Mandevilla scabra (Hoffmanns. ex Roem. & Schult.) K. Schum. and Smilax irrorata Matt. ex Griseb. On more exposed, bare canga slabs, the plants grow mostly in rock crevices with presence of monocots such as Véllozia glauca Pohl, Sobralia liliastrum Salzm. ex Lindl., Dyckia duckei L.B. Sm. and the tuberous, low growing Mandevilla tenuifolia (J.C. Mikan) Woodson, as Plant beta diversity of canga outcrops 15 well as the herbaceous Borreria semiamplexicaulis E.L.Cabral, Perama carajensis J.H..Kirk.*, Begonia humilis Dryand and Brasilianthus carajensis Almeda & Michelangeli*. The nodular canga has more or less continuous covering of grass and sedge, with occasional specimens of Riencourtia pedunculosa (Rich.) Prusky. During the expeditions we did not come across low forest groves, and our impression was that between the canga edge and the surrounding rainforest there was not much transition but a sharp substitution of the open vegetation by the associated forest types. Regarding the hydromorphic vegetation found in SFX, temporary shallow ponds with Utricularia species, Burmannia flava Matt., Cabomba furcata Schult. & Schult. £., Syngonanthus caulescens (Poir.) Ruhland and Xyris brachysepala Kral.* were visited. However, perennial, larger ponds of the magnitude found in the Serra Sul were lacking and temporary streams were not observed. There were also Palm swamps (buritizais), with margins occupied by Mauritia flexuosa Matt. and Mauritiella armata (Mart.) Burret, harbouring aquatic Oryza glumaepatula Steud., Helanthium tenellum (Matt. ex Schult. & Schult.f.) Britton and Eleocharis spp. (edaphic endemic species marked with *). Database of the flora of Serra dos Carajas complex The biogeographical database from the CRC of the Carajas complex was updated by our study (see supplementary data) and includes now a total of 893 angiosperms distributed in 121 families and 441 genera. For the Carajas flora (FCC), Poaceae was the most species-rich family (75 species in the FCC), followed by Fabaceae (66 spp.), Cyper- aceae (57 spp.), Rubiaceae (49 spp.), and Melastomataceae (40 spp.). The richest genera were Rhynchospora (24 spp.), Miconia (18 spp.), Paspalum and Solanum (17 spp. each), Myrcia and Ipomoea (13 spp. each), while 64% (284 genera) were represented by only a single species. The inclusion of SFX in our database increased the number of known taxa by 18 genera and 37 species not previously recorded for the canga of Carajas. Biogeography of the Campos Rupestres on Canga of the Carajas complex The mean angiosperm species richness for each outcrop of the Serra dos Carajas was 218 species. The NMDS and UPGMA analyses included 3451 records of 893 species across 16 sites (Fig. 3a, b). The UPGMA analyses produced statistically significant clusters (Fig. 3b) with the same major groups found by Fonseca-da-Silva et al. (2020), one comprising four of the eight areas of the Serra Norte (SN2, SN6, SN7, and SN§8), while the remaining four (SN1, SN3, SN4, and N5) appear closer to the areas of Serra Sul (SILA, S11B. S11C, S11D), along with SB and ST. SA also emerged as the least similar to the Carajas complex, and SFX was found to be more similar to the group comprising SB, ST, Serra Sul and the four most species rich sites in Serra Norte (SN1, SN3, SN4, and SN5). A similar result was obtained by the NMDS analysis (Fig. 3a), also showing SA as the most dissimilar from other areas. 16 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) NMDS comparing the Iron islands in the Amazon UPGMA grouping @ara SN6 @sn2 SN8 4000 - - - 0.6000 -0.4500 -0.3000 -0.1500 0.0000 0.1500 0.3000 0.4500 @ Serra Arqueada @ Serra de Sao Felix do Xingu @Serra Sul @Serra Norte @Serrada Bocaina © Serra do Tarzan Figure 3. UPGMA (a) and NMDS (b) multivariate analysis clustering areas from FCC and SFX (see Table 2 for area codes). UPGMA cophenetic coefficient: 0.902. b. NMDS stress: 0.1859. 3 a 8 3 Richness 6 Total number of shared species “ Total number of shared endemic species 200 é 5 10 45 20 0 50 100 150 0 50 100 160 a a Area (km?) i b Distance (km) Cc Distance (km) Figure 4. a Species richness plotted against area of Carajas. Pearson correlation coefficients: 7 = 0.806094, P = 0.001548 b the number of species shared between site pairs does not change significantly with geo- graphical distance between regions. r = -0.16; P = 0.08 ¢ the number of shared endemic species between site pairs declines with geographical distance between regions. r= -0.45872; P = 1.37e-07. Species richness was significantly correlated with site area (7 = 0.806094, P= 0.001548). The larger the area of each individual mountaintop (site), the larger the number of spe- cies recorded. The total number of shared species between mountaintop outcrops did not differ significantly with geographical distance across sites (7 = -0.16; P = 0.08). There was a tendency of distant sites to share less species, but this trend was not significant. When the residuals of this model were evaluated they significantly departed from normality. Spearman's correlation was not significant either (p-value = 0.2972). However, when fo- cusing on the number of shared endemic edaphic species versus the geographical distance between sites, we found a significant correlation, where closer sites shared more edaphic endemic species than with more distant sites (7 = -0.45872; P = 1.37e-07) (Fig. 4). Plant beta diversity of canga outcrops is Regarding the total of species of the canga, the Carajas iron islands share an average of 40% of their flora with each other. SFX has, on average, 30% of shared species with each other area. The percentage of similarity between sites was a minimum of 30% and a maximum of 55%. Discussion Floristic composition of Serra de Campos X other canga outcrops The most species-rich families and genera found in the SFX coincide with those found in the Flora das cangas de Carajas (Mota et al. 2018) and SA (Fonseca-da-Silva et al. 2020), where Cyperaceae, Fabaceae, Poaceae, and Rubiaceae are among the rich- est plant families. Interestingly, SFX has a much higher number of Orchidaceae spe- cies than other surveys of canga in the Amazon (Koch et al. 2018; Mota et al. 2018; Fonseca-da-Silva et al. 2020). The participation of botanical specialists during collect- ing expeditions enhances floristic studies in the Amazon (Medeiros et al. 2014) and elsewhere, and the high number of Orchidaceae in SFX possibly reflects the specific search for this group by J.B. Silva in the region from the 1990’s onwards, which may have resulted in a greater sampling effort for this group when compared to other areas. There is a large turnover of species between outcrops (Zappi et al. 2019; Fonseca- da-Silva et al. 2020) and very few species are widely distributed across these disjunct, isolated habitats. Similar to what was found by (Costa et al. 2019) in Amazonian White Sand Campinas, the isolation of the patchy canga outcrops limits dispersal and increases floristic differentiation, and the adverse conditions, such as high temperature, extreme exposure to sunlight and winds, and a relatively well defined dry season repre- sent ecological filters for the species that occupy the canga, partly explaining the high number of endemic species in the CRC of Carajas. As an example, only three species were recorded in all surveyed areas: the widely distributed Riencourtia pedunculosa, an Asteraceae common in open areas in the Amazon (Flora do Brasil under construction, Bringel 2014), and two species associated with Ama- zonian canga outcrops: Brasilianthus carajensis and Perama carajensis. Perama carajensis is a confirmed canga edaphic endemic species, and Brasilianthus carajensis has been collected also on granite, being locally endemic to Carajas, but not a canga edaphic endemic (Giuli- etti et al. 2019; Silva et al. 2020). Other four species also present wide occurrence across campos rupestres on canga of Carajas: Bulbostylis conifera (Kunth) C.B. Clarke, Rhynchospora barbata (Vahl) Kunth, Rhynchospora seccoi C.S.Nunes et al., and Syngonanthus discretifolius (Moldenke) M.T-C. Watanabe were recorded for SFX and many other FCC areas, except for one of them missing in SN3, SN7, SN7 and SA, respectively. Their absence in these four sites may be related to the more modest canga surface found in these areas. Some widely distributed species from the canga of Carajas, found at more than 10 of the 16 sites surveyed, were not recorded at SFX. The absence of the common treelets Callisthene microphylla Warm. and Mimosa acutistipula var. ferrea Barneby (Mota et al. 18 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) 2015) at SFX may be partially explained by differences in the micro-habitats between SFX and the other canga outcrops considered here. For Brasilianthus carajensis, distinct adaptive genetic clusters have been found in the SFX (see Silva et al. 2020), increasing the argument for the protection of the site. The canga is typically a mosaic of different vegetation types (Mota et al. 2015, Vi- ana et al. 2016). Some of these vegetation types are infrequent in SFX, as for example low forest groves (Mota et al. 2015), and in consequence some of the species found in these groves elsewhere are absent at SFX: Callisthene microphylla, Mimosa acutistipula vat. ferrea, and Cereus hexagonus (L.) Mill. Although forest groves are closely associated with the lower scrub vegetation, the latter is more abundant in the canga plateau of SFX than the former. In plateau SFX2 of SFX the shrubby vegetation is dominant, and there are large stands of Syagrus cocoides Mart., a palm emerging from the impenetrable shrubbery. In the context of CRC of Carajas, this palm forms large populations only in SA and SFX. Despite having the lowest number of species registered in the FCC, the hydromorphic vegetation found atop the plateaus is the habitat with the highest proportion of exclusive species (Pereira et al. 2016; Mota et al. 2018). Seasonal lakes and palm lakes in the SFX en- sure the presence of annual aquatic species such as Eriocaulon carajense Moldenke, Oryza glumaepatula Steud., Syngonanthus caulescens (Poir.) Ruhland, and Xyris brachysepala Kral. As a relatively large canga site isolated from the active iron mines further to the east, the SFX has been found to harbour a rich and unique vegetation, representing a suitable area for the implementation of conservation strategies. On the other hand, this canga outcrop is currently threatened by surrounding deforestation, land transforma- tion and frequent fires, and is not included within any type of protected area. lron islands of Carajas and their floristic connections The mosaic of landscapes typical of CRC of Carajas may also explain the low floristic similarity between the sites. The number of shared species represents less than half the local richness from each site separately. This brings attention to the high beta diversity among sites (Zappi et al. 2019), with a large species turnover across these disjunct out- crops. Habitat diversity associated with the size of the island-like habitats is also related to the beta diversity in French Guiana’s inselbergs (Henneron et al. 2019), similarly to what is found in Andean alpine flora (Sklenaf et al. 2014) and South American tepuis (Riina et al. 2019). This confirms the association between area and habitat diversity found here for the canga vegetation as an important factor for determining plant biodiversity. The greater similarity between SFX, SB and ST, along with Serra Sul (S11A, S11B, S11C, and $11D) and SN1, SN3, SN4 and SN5 reflected in the UPGMA clustering patterns (Fig. 3b) suggests there is more similarity of species richness between the largest sites rather than among geographically closest areas, as observed by Fonseca-da-Silva et al. (2020) for SA. In fact, the correlation between the shared species of each canga site and their geographical distance was significant. Considering the size of each of these ar- eas and their positive correlation with floristic richness (Fig. 4), we interpret the canga $ Plant beta diversity of canga outcrops 19 overall surface as being more important for floristic composition than the distance be- tween sites in the Serra dos Carajas. Thus, the larger a canga outcrop is, the greater the number of micro-habitats it can harbour, reflecting an increased species richness and unique floristic composition of each canga site. On the other hand, that relationship (distance between areas vs shared flora) holds true when analysing shared endemic spe- cies, where shared endemic species decrease with distance at different rates (Fig. 4C). The low number of species restricted to the Amazon (25%) and the high number of species widely distributed in South America (75%) recorded at SFX, may explain the discrepancy in the correlation between shared species and distance being negative when all species are considered, whereas it is positive for endemic species only. On a macro-scale, the majority of the species recorded in SFX have a broad distribution, oc- curring beyond the Amazon Rainforest, and the distance factor between different out- crops may not matter so much. On the other hand, when observing only the species endemic to Carajas, and especially edaphic endemic species, the trend is the opposite, possibly due to the local scale of observation, as elsewhere the distance between areas tends to affect the floristic similarity between island vegetations (Sklenaf et al. 2014; Schrader et al. 2020). A genomic study revealed that gene flow in two endemic species of Carajas is mainly influenced by geographic distance between mountain pairs, as the rainforest surrounding different mountaintops constitutes an important barrier (Car- valho et al. 2019). Therefore, gene flow also decreases with the increase of the barrier represented by the rainforest (Carvalho et al. 2019). Another factor that may have an impact on the contrasting effects of floristic simi- larity vs. distance from canga islands is the different environmental requirements of herbs, shrubs and trees, that shape their biogeographical patterns and affect species- area and richness-environment relationships (Schrader et al. 2020). Herbs, shrubs and trees have contrasting strategies in different environmental conditions with potential implications for community assemblage on islands. For example, herbs can form larger populations on small islands due to their smaller size, and as a result face less risk of extinction and greater dispersal capacity (Moles 2005; Thomson et al. 2010), while shrubs are associated with more stable environmental conditions, and therefore have more success on larger islands (Chiarucci et al. 2017). Recent analyses of open vegetation in the Amazon reinforce the insular character of Amazonian canga and their low similarity to other vegetation types in the Amazonian biome (Devecchi et al. 2020). While there is some evidence that canga in Southeastern Brazil may be influenced by the surrounding Atlantic Rainforest and Cerrado (Zappi et al. 2017) these biomes are known to have a more varied life-form balance (respectively 1: 4 and 1: 7 proportion of trees over other life forms) than the Amazon Rainforest, where the life form balance is less extreme (1: 2) (Brazil Flora Group [BFG] 2015), thus it may have less floristic influence over the open vegetation found in the CRC of Carajas (Zappi et al. 2019). Therefore, in order to colonize the Amazonian CRC, shrubby or herbaceous plant species may have to come from further afield through long distance dispersal, and, if established, they may remain genetically isolated from their original populations, leading over a period of time to the patterns of endemism observed today. 20 Caroline Oliveira Andrino et al. / PhytoKeys 165: 1-25 (2020) Different evolutionary processes of the species occurring in CRC may also have led to different floristic composition in the outcrops. Although evolutionary studies involv- ing species of canga in the Brazilian Amazon are just beginning (Zappi et al. 2017), the phylogeography of a species of Gesneriaceae distributed in humid rock formations in the Cerrado reveals its recent expansion into CRC vegetation during the Pleistocene (Fiorini et al. 2020). Recent and rapid radiations have been observed in mountaintops ecosystems (Salerno et al. 2012; Pirie et al. 2016; Vasconcelos et al. 2020) but more phylogenetic and phylogeographic studies are necessary to establish dating for plants species groups found in the CRC in order to understand their diversification and colonization processes. Table 3. Species richness of the iron islands outcrops of Carajas complex (bold diagonal) along with the number of shared species (above diagonal) and distance in kilometres (below diagonal) between the centroid sites; an estimated area for each site is provided. Sites Area SB ST ARQ SI1IA S11B S11C S11D SFX SN1 SN2 SN3 SN4 SN5 SN6 SN7_ SN8 (km’) SB 19.98 221 100 47 79 80 75 135 85 124 46 84 108 101 56 57 56 ST 8.3 24 209 48 88 90 80 138 84 119 59 87 102 105 55 59 53 ARQ 1.27. 140 116 149 52 44 45 80 70 75 30 52 77 62 30 29 32 S11A 15.27 59 24 92 228 139 119 170 96 143 59 89 116 101 56 54 53 SIIB 844 546 308 82 45 199 107 147 77 120 53 81 96 99 49 52 48 S11C 6.26 52.5 28.8 85 10 45 177 140 83 110 46 72 101 91 49 41 50 S11D 1641 47 244 92.3 15.7. 9.8 5.7 424 141 222 80 134 189 168 75 80 72 SFX 9.04 217 193 79.5 158 162 165 170 239 131 48 82 lll 95 52 44 51 SNI 211.81 52 37.7 Ill +37 38 40 42 180 381 98 154 183 174 77 71 78 SN2 0.86 46.8 32.8 113 368 37.1 39.3 40 184 518 124 69 73 71 40 34 44 SN3. 2.1 44.7 32 117.5 40.2 40.1 42 42.2 188 81 3.8 217 129 103 71 60 59 SN4 14.83 38 25. 117.4 37.55 364 37.7 37 189 13.7 86 74 305 181 74 65 81 SN5 8.26 32.36 22.75 122 41 39 40 38.53 195 19.78 14.6 12.4 6.2 289 63 54 69 SNG . 0°97 35:29 22.46" 108, “37.3 35:8 936.7 "35.7 190% 46 11 10 3 4 99 40 42 SN7 0.34 33 19 117 35.7 33.8 34 33.1 190.5 18 14 13 6 5 3 112 46 SN8 2.69 30 17) AIG 37" = 347. 35 oo a MDZ ae 22. 17 16 8.8 6 5.7 3.3100 Table 4. Endemic edaphic species of the iron islands outcrops of Carajas complex (bold diagonal) along with the number of shared endemic species (above diagonal) and distance in kilometres (below diagonal) between the centroid sites. Sites SB ST ARQ SIIA S11B S11C S11D SFX SN1 SN2 SN3 SN4 SNS SNG SN7_ SNB8 SB 20 15 3 17 15 16 19 11 18 11 15 15 13 11 11 12 ST 24 16 2 14 13 14 15 9 15 9 12 11 11 9 10 10 ARO I40u WUl6me ax mite Oa “Bel ees Us es ore as dy S11A 59 24 92 24 17 21 22, 14 21 10 16 17 13 11 9 12 S11B 54.6 30.8 82 4.5 18 18 19 10 15 14 14 13 12 10 8 10 S11C 52.5 28.8 85 10 4.5 21 21 13 11 10 15 15 13 10 9 12 $11D 47 24.4 92.3 15.7 9.8 5.7 25 14 21 11 18 19 14 12 12 14 SFX 217 193 79.5 158 162 165 170 17 13 9 13 12 8 9 7 9 SN1 52 37.7 111 37 38 40 42 180 29 15 20 29, 19 13 12 16 SN2 46.8 32.8 113 368 37.1 39.3 40 184 5.18 16 15 14 14 11 8 12 SN3 44.7 32 »=117.5 40.2 40.1 42 42.2 188 8.1 3.8 23 20 15 15 12 15 SN4 38 25 117.4 37.5 364 37.7 37 189 = 13.7 8.6 7A 24 18 14 12 17 SN5 = 32.36 22.75 122 41 39 40 38.53 195 19.78 146 12.4 6.2 20 11 9 15 SN6 35.29 22.46 118 373 35.8 36.7 35.7 199 16 11 10 3 4 SNiee Se eLOTE LI? 85%, Biel 3h 95350 wl905- 18 Si wis, “6 “5. mse Bade) Lin SN8 30 17 119 37 34.7 35 33 192 22 17 16 8.8 6 Plant beta diversity of canga outcrops ZA Conclusions This is the most complete study analysing a database of canga outcrop islands in the Amazon thus far. Our data suggest higher shared similarity between largest sites and higher species richness. We show that species richness in these vegetation islands re- veals complex biogeographic patterns and relatively high beta diversity. Outcrop size seemed to be more important than geographical proximity between outcrops, and this should be taken into account when drafting conservation and compensation measures for the canga. There are still inaccessible canga outcrops towards the north of the state of Para that remain unexplored, and their study would certainly yield interesting infor- mation to be added to the present findings. Acknowledgements We are grateful to the Museu Paraense Emilio Goeldi (MPEG) and Instituto Tec- noldgico Vale (ITV) for essential infrastructure and support for this project, and to Priscila O. Rosa, from the Herbarium HEPH, for providing specimen images. We also acknowledge the financial support provided by the Conselho Nacional de Desenvolvimento Cientifico e Tecnolédgico (CNPq) for grants for COA and RGBS, and CAPES (JL). DCZ currently holds a research grant from CNPq. Invaluable help was provided by specialist botanists Aline Stadnik, Ana Carolina Mezzonato, Beatriz Gomes, Edgar Afonso, Edley Pessoa, Jovani Pereira, Layla Schneider, Matheus Cota, Mayara Pastore, Paulo Gonella, and Valdir Silva-Junior in specimen naming. We thank Nigel P. Taylor for revising the English. We also thank our colleague Alice Hiura for technical support and Fernando Marino Gomes dos Santos for critical reading. Data availability statement: All supplementary data can be accessed at figshare repository: https://doi.org/10.6084/m9.figshare. 12053487 References Ab’saber AN (1986) Geomorfologia da regido. In: Almeida JMG (Ed.) Carajas: desafio politico, ecologia e desenvolvimento. CNPq, Brasilia, 88-124. 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