The pattern of high plant diversity of Neotropical inselbergs: highlighting endemic, threatened and unique species

Herval Vieira Pinto-Junior Pedro Manuel Villa Miriam Cristina Alvarez Pereira Luis Fernando Tavares de Menezes About the authors

ABSTRACT

Understanding how multiple drivers shape plant community diversity across environmental gradients is one of the most important issues in plant ecology and biodiversity conservation. We aimed to analyse plant community structure and diversity in four inselbergs in Espírito Santo State, Brazil. We evaluated species diversity, floristic composition and similarity, phytosociological structure, occurrence, and conservation status of rupicolous flora in the inselberg communities. We used field expeditions and plant inventory data from 370 sampling units. We estimated floristic similarity and compared diversity indexes among inselbergs. We observed marked differences in community structure and diversity among inselbergs, where the southern region had the highest number of taxa and higher values of diversity indices. There were also notable differences in floristic composition and phytosociological structure, with a decrease in similarity as geographical distance increased. This finding demonstrated the existence of differences in the patterns of dominance and vegetation cover along the latitudinal gradient, as well as differences in endemic, threatened, and exclusive species, and represents a first step toward establishing criteria for biodiversity conservation for inselbergs in Espírito Santo State.

Keywords:
alpha diversity; Atlantic Forest; biodiversity conservation; floristic composition; latitudinal gradient; phytosociological structure; rock outcrop

Introduction

Inselbergs are usually rocky granite outcrops that emerge abruptly from their surrounding ecosystems, such as savannah and forests, representing isolated terrestrial islands (Porembski & Barthlott 2000Porembski S, Seine R, Barthlott W. 2000b. Factors Controlling Species Richness of Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 49-66. ; Parmentier & Hardy 2009Parmentier I, Hardy OJ. 2009. The impact of ecological differentiation and dispersal limitation on species turnover and phylogenetic structure of inselberg’s plant communities. Ecography 32: 613-622. ). These rocky outcrops are common around the world, occurring in America, Africa, Asia, and Australia (Carlucci et al. 2014Carlucci MB, Bastazini VAG, Hofmann GS, et al. 2014. Taxonomic and functional diversity of woody plant communities on opposing slopes of inselbergs in southern Brazil. Plant Ecology & Diversity 8: 187-197. ), and form important landscape elements that play a role in the maintenance of biodiversity (Porembski et al. 2016Porembski S, Silveira FAO, Fiedler PL, et al. 2016. Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodiversity and Conservation 25: 2827-2830. ). Inselbergs lato sensu are found throughout the east of Brazil, from the north-eastern semi-arid region to the cloudy and cold highlands of Rio Grande do Sul (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ). Although these granite outcrops are recognised by 75 % of the Brazilian population, they are still poorly studied; neither the floristic characteristics nor the ecological and biogeographical features of the flora are widely known (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ). Even with a few studies, the inselbergs in south-eastern Brazil, mainly in the states of Espírito Santo, Minas Gerais, and Rio de Janeiro, have the greatest expression of vegetation variability (Moura et al. 2011Moura IO, Ribeiro KT, Takahasi A. 2011. Amostragem da vegetação em ambientes rochosos. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA, Meira-Neto JAA. (eds.) Fitossociologia no Brasil: Métodos e estudos de casos. Viçosa, Editora UFV. p. 255-294.; de Paula et al. 2020de Paula LFA, Azevedo LO, Mauad LP, et al. 2020. Sugarloaf Land in southeastern Brazil: a tropical hotspot of lowland inselberg plant diversity. Biodiversity Data Journal 8: e53135. doi: 10.3897 / BDJ.8.e53135
https://doi.org/10.3897 / BDJ.8.e53135...
).

The most-studied domains with inselbergs in Brazil are the Atlantic Forest, the Cerrado, and the Caatinga. These areas have a mosaic of vegetation types, where the union between biotic and physical factors results in the most diverse and heterogeneous inselbergs (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ). In this context, the sharing of flora among inselbergs will depend on their specific environmental conditions and the degree of isolation (Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ), which can change over relatively short distances (Schut et al. 2014Schut AGT, Wardell‐Johnson GW, Yates CJ, et al. 2014. Rapid characterization of vegetation structure to predict refugia and climate change impacts across a global biodiversity hotspot. PLOS ONE 9: e82778. doi: 10.1371/journal.pone.0082778
https://doi.org/10.1371/journal.pone.008...
) and provide heterogeneity to support plant diversity (Yates et al. 2019Yates CJ, Robinson T, Wardell‐Johnson GW, et al. 2019. High species diversity and turnover in granite inselberg floras highlight the need for a conservation strategy protecting many outcrops. Ecology and Evolution 9: 7660-7675.). Even with few and specific studies carried out in Espírito Santo State (Esgario et al. 2009Esgario CP, Fontana AP, Silva AG. 2009. A flora vascular sobre rocha no Alto Misterioso, uma área prioritária para a conservação da Mata Atlântica no Espírito Santo, Sudeste do Brasil. Natureza Online 7: 80-91.; Couto et al. 2016Couto DR, Dias HM, Pereira MCA, Fraga CN, Pezzopane JEM. 2016. Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops (inselbergs) in Brazilian Atlantic Rainforest: basis for conservation of a threatened ecosystem. Rodriguésia 67: 583-601. ; 2017Couto DR, Francisco TM, Manhães VC, Dias HM, Pereira MCA. 2017. Floristic composition of a Neotropical inselberg from Espírito Santo state, Brazil: an important area for conservation. Check List 13: 2043. doi: doi.org/10.15560/13.1.2043
https://doi.org/doi.org/10.15560/13.1.20...
; 2019Couto DR, Francisco TM, Garbin ML, et al. 2019. Surface roots as a new ecological zone for occurrence of vascular epiphytes: a case study on Pseudobombax trees on inselbergs. Plant Ecology 220: 1071-1084. ; Francisco et al. 2018Francisco TM, Couto DR, Evans DM, et al. 2018. Structure and robustness of an epiphyte-phorophyte commensalistic network in a neotropical inselberg. Austral Ecology 43: 903-914. ; Pena & Alves-Araújo 2017Pena NTL, Alves-Araújo A. 2017. Angiosperms from rocky outcrops of Pedra do Elefante, Nova Venécia, Espírito Santo, Brazil. Rodriguésia 68: 1895-1905. ; Pinto-Junior et al. 2020Pinto-Junior HV, Villa PM, Menezes LFT, Pereira MCA. 2020. Effect of climate and altitude on plant community composition and richness in Brazilian inselbergs. Journal of Mountain Science 17: 1931-1941. ), the granitic inselbergs were listed as priority areas for conservation (Martinelli 2007), and have been described as vegetation relicts and ecological refuges (IBGE 2012IBGE. 2012. Manual Técnico da Vegetação Brasileira. 2nd. edn. Rio de Janeiro, Instituto Brasileiro de Geografia e Estatística.). However, these inselbergs are threatened, mostly due to exploration and trading ornamental rocks (Campello 2000Campello MS. 2000. Caracterização tecnológica de granitos ornamentais. Msc. Thesis, Universidade Federal de Minas Gerais, Belo Horizonte.).

Despite the recognized value for conservation, granitic inselbergs also have characteristics such as reduced dispersability (Hopper et al. 2009Hopper SD. 2009. OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322: 49-86.), high numbers of localized rare/endemics species (Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ) and strongly differentiated population systems (Hmeljevski et al. 2017Hmeljevski KV, Nazareno AG, Bueno ML, Reis MS, Forzza RC. 2017. Do plant populations on distinct inselbergs talk to each other? A case study of genetic connectivity of a bromeliad species in an Ocbil landscape. Ecology and Evolution 7: 4704-4716. ), which can assist to develop hypotheses explaining the ecology, evolution and best conservation practices for very old, climatically buffered and infertile landscapes (Ocbil theory) (Hopper et al. 2016Hopper SD, Silveira FAO, Fiedler PL. 2016. Biodiversity hotspots and Ocbil theory. Plant and Soil 403: 167-216. ). Thus, there are still large gaps in our knowledge regarding the flora and ecological processes of various mountain regions throughout the Brazilian territory, including the inselbergs (Meirelles et al. 1999Meirelles ST, Pivello VR, Joly CA. 1999. The vegetation of granite rock outcrops in Rio de Janeiro, Brazil, and the need for its protection. Environmental Conservation 26: 10-20. ; Martinelli 2007Martinelli G. 2007. Mountain biodiversity in Brazil. Brazilian Journal of Botany 30: 587-597. ).

Understanding how multiple drivers shape plant community diversity across environmental gradients is one of the most important issues in plant ecology and biodiversity conservation (Lavergne et al. 2010Lavergne S, Mouquet N, Thuiller W, Ronce O. 2010. Biodiversity and Climate Change: Integrating Evolutionary and Ecological Responses of Species and Communities. Annual Review of Ecology, Evolution, and Systematics 41: 321-350. ). However, how the plant community is structured on tropical inselbergs remains unknown; data on species diversity and phytosociological structure are especially sparse. The geological, geomorphological and microenvironmental characteristics of inselbergs provide extreme environmental conditions (i.e. low nutrient or water availability, high radiation levels and large temperature amplitude); only certain plant species, with morphological and ecophysiological adaptations, can tolerate such conditions (Lüttge 1997Lüttge U. 1997. Physiological ecology of tropical plants. Berlín, Heidelberg, Springer Verlag. ; Bremer & Sander 2000Bremer H, Sander H. 2000. Inselbergs: Geomorphology and Geoecology. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer Verlag . p. 7-34. ; Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ). These species consequently have a restricted geographic distribution with a considerable number being endemics (Barthlott et al. 1993Barthlott W, Gröger A, Porembski S. 1993. Some remarks on the vegetation of tropical inselbergs: diversity and ecological differentiation. Compte rendu des Séances de la Société de Biogéographie 69: 105-124.; Porembski et al. 2000Porembski S, Becker U, Seine R. 2000 a. Islands on Islands: Habitats on Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 49-66. a; Seine et al. 2000Seine R, Porembski S, Becker U. 2000. Phytogeography. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 435-448. ; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ) and predominantly create patchy vegetation formations (Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ; de Paula et al. 2016de Paula LFA, Forzza RC, Neri AV, Bueno ML, Porembski S. 2016. Sugar Loaf Land in south-eastern Brazil: a centre of diversity for mat-forming bromeliads on Inselbergs. Botanical Journal of the Linnean Society 181: 459-476. ; Villa et al. 2018Villa PM, Gastauer M, Martins SV, et al. 2018b. Phylogenetic structure is determined by patch size in rock outcrop vegetation on an inselberg in the northern Amazon region. Acta Amazonica 48: 248-256. b).

In this study, we aimed to analyze the plant community structure and diversity in four inselbergs in Espírito Santo State, south-eastern Brazil. Specifically, we evaluated the plant species diversity, floristic composition and similarity, phytosociological structure, and the occurrence and conservation status of rupicolous flora on inselbergs. As a consequence, our knowledge of plant community structure and diversity patterns on the inselbergs can be used to increase the likelihood of success in defining conservation criteria.

Materials and methods

Study Areas

This study was performed on four inselbergs located in the Atlantic Forest matrix in Espírito Santo State, south-eastern Brazil (Fig. 1, Tab. 1). This rupicolous vegetation is typical of Espírito Santo, being associated with granitic and gneissic inselbergs, and can be found between 0 and 1,480 m a.s.l. The vegetation is mainly associated with plant communities formed by monocotyledonous mats of Bromeliaceae, Cyperaceae, and Velloziaceae distributed in patches and/or shrubs (Porembski et al. 2000Porembski S, Becker U, Seine R. 2000 a. Islands on Islands: Habitats on Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 49-66. a; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ).

Figure 1
Location and general aspects of the study area. A - Location of the study area in relation to South America and B - in relation to Brazil and Espírito Santo State (ES). Border states: BA - Bahia, MG - Minas Gerais and RJ - Rio de Janeiro. Study area: white square - Pedra do Elefante, white circle - Águia Branca (north), white triangle - Forno Grande and white cross - Pedra de Pontões (south).

Table 1
General descriptions of four Neotropical inselbergs selected in Espírito Santo State, south-eastern Brazil.

Vegetation sampling

The line intercept transect method was used to measure coverage for all plants (Mueller-Dombois & Ellenberg 2002Mueller-Dombois D, Ellenberg H. 2002. Aims and Methods of Vegetation Ecology. New Jersey, The Blackburn Press.; Herrick et al. 2017Herrick JE, Zee JW, McCord SE, et al. 2017. Monitoring Manual for Grassland, Shrubland and Savanna Ecosystems. Las Cruzes, New Mexico, USDA-ARS Jornada Experimental Range.; Morgan & Salmon 2019Morgan JW, Salmon KL. 2019. Dominant C3 tussock grasses are resilient to the re‐introduction of fire in long‐unburned temperate grasslands. Applied Vegetation Science 23: 149-158. ). The cover was measured along a line intercept transect, by noting the point along with the tape where the cover began and the point at which it ended (Elzinga et al. 2001Elzinga CL, Salzer DW, Willoughby JW. 2001. Field Techniques for Measuring Vegetation. In: Elzinga CL, Salzer DW, Willoughby JW. (eds.) Measuring & Monitoring Plant Populations, Denver, Colorado, Bureau of Land Management. p. 181-182.). In each inselberg, ten parallel 100 m lines, systematically spaced at 10 m, were used for recording plant coverage. Every intercept was divided into 10 m intervals to determine the beginning and the end of each sampling unit, and then, the frequency of occurrence of each species (Elzinga et al. 2001Elzinga CL, Salzer DW, Willoughby JW. 2001. Field Techniques for Measuring Vegetation. In: Elzinga CL, Salzer DW, Willoughby JW. (eds.) Measuring & Monitoring Plant Populations, Denver, Colorado, Bureau of Land Management. p. 181-182.; Mueller-Dombois & Ellenberg 2002Mueller-Dombois D, Ellenberg H. 2002. Aims and Methods of Vegetation Ecology. New Jersey, The Blackburn Press.; Herrick et al. 2017Herrick JE, Zee JW, McCord SE, et al. 2017. Monitoring Manual for Grassland, Shrubland and Savanna Ecosystems. Las Cruzes, New Mexico, USDA-ARS Jornada Experimental Range.). Sampling points with bare rock were removed from the analysis.

Floristic survey

The floristic survey consisted of the collection of fertile specimens and was conducted between April 2015 and July 2019, with successive field expeditions to encompass the different seasons. All fertile botanical material was collected and processed according to the usual techniques for vascular plants (Fidalgo & Bononi 1989Fidalgo O, Bononi VLR. 1989. Técnicas de coleta, preservação e herborização de material botânico. São Paulo, Governo do Estado de São Paulo, Secretaria do Meio Ambiente, Instituto de Botânica.). Taxonomic identification of botanical material was carried out by using the Flora do Brasil 2020 em construção (2020)Flora do Brasil 2020 em construção. 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/. 15 Out. 2019.
http://floradobrasil.jbrj.gov.br/...
, taxonomic literature, herbarium data, and expert taxonomists. All botanical material was deposited in the herbariums of the Universidade Federal do Espírito Santo (SAMES, CAP, and VIES), Instituto Nacional da Mata Atlântica (INMA/MBML) and Universidade Federal de Viçosa (VIC), with duplicate samples sent to the herbarium of Jardim Botânico do Rio de Janeiro (RB). The spelling of names, synonymy, and authors follow Flora do Brasil 2020 em construção 2020 (JBRJ 2019JBRJ - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. 2019. Flora do Brasil 2020 em construção. Rio de Janeiro. http://floradobrasil.jbrj.gov.br. 10 Jun. 2019.
http://floradobrasil.jbrj.gov.br...
) with APG IV (2016)APG IV - The Angiosperm Phylogeny Group. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20. circumscription for angiosperm families, and PPG I (2016)PPG I - Pteridophyte Phylogeny Group I. 2016. A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563-603. for monilophytes and lycophytes. Species life forms were classified according to Raunkiaer (1934Raunkiaer C. 1934. The life forms of plants and statistical geography. Oxford, Clarendon.).

Quantification of biodiversity indexes

Measurements of taxonomic diversity indices were calculated in each sampling area along the climatic gradient. Measurements included species richness, Shannon-Wiener and Pielou evenness index (Magurran 2004Magurran AE. 2004. Ecological diversity and its measurement. New Jersey, Princeton University Press.). Species richness refers to the total number of species recorded at each sampled area. The Shannon-Wiener index (H’) and Pielou evenness index (J) were calculated using the following equations:

H = p i . l n ( p i )

and

J = H / H m a x

where pi is the absolute coverage of each species; ln is the natural logarithm; H’max is ln of S and S is the total number of species at a sampling area. These indices incorporate the species richness and the proportion of each species within each sample (Magurran 2004Magurran AE. 2004. Ecological diversity and its measurement. New Jersey, Princeton University Press.). All diversity indices were calculated using the ‘vegan’ package (Oksanen et al. 2019Oksanen J, Blanchet FG, Friendly M, et al. 2019. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan. 20 Jan. 2020.
https://CRAN.R-project.org/package=vegan...
) in R software 4.0.3 (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. 20 Jan. 2020.
https://www.R-project.org/...
).

Data analyses

To test the floristic similarity between the four sampled areas, a Cluster Analysis was performed using a matrix of presence and absence data, using Sørensen Distance as the coefficient and UPGMA as the algorithm. The inclusion criterion of individuals in the matrix was the identification at the species level. The cluster analysis was represented by a similarity matrix and was evaluated by the Cophenetic Correlation Coefficient (CCC).

Measures of alpha diversity were calculated for each sampling area by site using species richness, Pielou evenness and Shannon-Wiener diversity index. To compare the means of cover and alpha diversity metrics, we performed the Kruskal-Wallis test (for non-normally distributed data), followed by Dunn’s multiple comparison test (Dinno 2017Dinno A. 2017. dunn.test: Dunn's Test of Multiple Comparisons Using Rank Sums. R package version 1.3.5. https://CRAN.R-project.org/package=dunn.test. 20 Jan. 2020.
https://CRAN.R-project.org/package=dunn....
). Variables were tested for normal distribution with the Shapiro-Wilk test and by evaluating the Q-Q plot (Crawley 2012Crawley MJ. 2012. The R book. 2nd. edn. West Sussex, United Kingdom, John Wiley & Sons Ltd.). All these analyses were performed using the ‘ade4’, ‘car’, ‘cluster’, ‘dunn.test’, ‘gclus’, ‘permute’ and ‘vegan’ packages (Hurley 2019Hurley C. 2019. gclus: Clustering Graphics. R package version 1.3.2. https://CRAN.R-project.org/package=gclus. 20 Jan. 2020.
https://CRAN.R-project.org/package=gclus...
; Maechler et al. 2018Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K. 2018. cluster: Cluster Analysis Basics and Extensions. R package version 2.0.7-1. https://www.researchgate.net/publication/272176869_Cluster_Cluster_Analysis_Basics_and_Extensions. 20 Jan. 2020.
https://www.researchgate.net/publication...
; Oksanen et al. 2019Oksanen J, Blanchet FG, Friendly M, et al. 2019. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan. 20 Jan. 2020.
https://CRAN.R-project.org/package=vegan...
; Simpson 2019Simpson GL. 2019. permute: Functions for Generating Restricted Permutations of Data. R package version 0.9-5. https://CRAN.R-project.org/package=permute. 20 Jan. 2020.
https://CRAN.R-project.org/package=permu...
; Dinno 2017; Dray & Dufour 2007Dray S, Dufour A. 2007. The ade4 Package: Implementing the Duality Diagram for Ecologists. Journal of Statistical Software 22: 1-20.; Fox & Weisberg 2019Fox J, Weisberg S. 2019. An R Companion to Applied Regression. 3nd. edn. Thousand Oaks, CA, Sage Publications.) in the R 4.0.3 software environment (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. 20 Jan. 2020.
https://www.R-project.org/...
).

Phytogeography, endemism and threatened species

The distribution of species and endemism were analysed using the literature and online databases, as Flora do Brasil 2020 em construção 2020 (JBRJ 2019JBRJ - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. 2019. Flora do Brasil 2020 em construção. Rio de Janeiro. http://floradobrasil.jbrj.gov.br. 10 Jun. 2019.
http://floradobrasil.jbrj.gov.br...
), Herbário Virtual da Flora e de Fungos (INCT 2019INCT - Institutos Nacionais de Ciência e Tecnologia. 2019. Herbário Virtual de Plantas e dos Fungos. http://inct.florabrasil.net/en/herbario-virtual/. 25 Apr. 2019.
http://inct.florabrasil.net/en/herbario-...
) and JABOT (JBRJ/Jabot 2019 JBRJ/Jabot - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. 2019. - Banco de dados da flora brasileira. http://www.jbrj.gov.br/jabot. 15 Jun. 2019.
http://www.jbrj.gov.br/jabot...
). Information on threatened species was obtained through the ‘Lista Nacional Oficial de Espécies da Flora Ameaçadas de Extinção’ (MMA 2014MMA - Ministério do Meio Ambiente. 2014. Lista Nacional Oficial de Espécies da Flora Ameaçadas de Extinção. Portaria 443, de 17 de dezembro de 2014. Brasília, Ministério do Meio Ambiente.), ‘Livro Vermelho da Flora do Brasil’ (Martinelli & Moraes 2013Martinelli G, Moraes MA. 2013. Livro Vermelho da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://dspace.jbrj.gov.br/jspui/handle/doc/26. 25 Nov. 2019.
http://dspace.jbrj.gov.br/jspui/handle/d...
) and ‘Espécies da Flora Ameaçadas de Extinção no Estado do Espírito Santo’ (Simonelli & Fraga 2007Simonelli M, Fraga CN. 2007. Espécies da flora ameaçadas de extinção no estado do Espírito Santo - Vitória. Vitória, Instituto de Permacultura e Ecovilas da Mata Atlântica.).

Results

Floristic composition

Based on 228 records, a total of 168 species of vascular plants were found belonging to 51 families and 114 genera, including 1 lycophyte, 13 pteridophytes, and 154 angiosperms (six magnoliids, 59 monocots, and 89 eudicots) (Tab. 2). The richest family was Orchidaceae with 13 species, followed by Asteraceae and Bromeliaceae (12 spp. each), Melastomataceae (11 spp.), Cyperaceae (eight spp.), Araceae (seven spp.), Clusiaceae, Euphorbiaceae, Fabaceae, Malvaceae and Velloziaceae (six spp. each) and Cactaceae (five spp.). The richest genera were Anthurium (Araceae) and Clusia (Clusiaceae) with six species each, followed by Pleroma (Melastomataceae) with five, Alcantarea (Bromeliaceae) and Peperomia (Piperaceae) with four species each. Also, five species from the inselbergs studied were recently described as new to science, and eight were new records for the Espírito Santo State. The life-form spectrum showed a predominance of phanerophytes (67 spp. - 40 %), followed by chamaephytes (47 spp. - 28 %), hemicryptophytes (39 spp. - 23.2 %) and cryptophytes (12 spp. - 7.1 %) (more details List S1 in supplementary material).

Table 2
List of species recorded in four Neotropical inselbergs in Espírito Santo State, southeastern Brazil. Life-forms: Th - therophyte, Cr - cryptophyte, Hc - hemicryptophytes, Ch - chamephytes, Ph - phanerophayte. Phytogeographic Domains: Am - Amazônia, Ca - Caatinga, Ce - Cerrado, MA - Mata Atlântica (Atlantic Forest), Pam - Pampa and Pan - Pantanal. * - exclusive occurrence to inselbergs, ! - endangered species. In bold endemics species of Espírito Santo State.

Phytosociological structure

Regarding species richness, the southern areas, located at higher altitudes, were richer than the northern areas; the number of genera and families also followed this pattern, but with less-significant differences (Tab. 3).

Table 3
Table containing the results of phytosociological structure of the four communities studied in Espírito Santo State, Brazil.

Among the families richest in species, Cyperaceae and Velloziaceae stand out in three studied areas, and Asteraceae, Melastomataceae, Orchidaceae, and Poaceae, in two southern areas. The percentage of genera with only one species exceeded 90% in Águia Branca and Pedra do Elefante, and reached its highest value in Forno Grande; for families with only one species, the highest percentage was observed in Pedra de Pontões (Tab. 3). The total vegetation sampled from 1,000 linear meters was higher in the southern sites; consequently, the highest values for bare rock were recorded to northern areas of Espírito Santo State.

The four plant communities were organized in an oligarchic structure, where a few species dominant account more than 50 % of the Importance Value (IV). In Águia Branca three species totaled 75.68 % of IV, Vellozia plicata, Trilepis lhotzkiana and Alcantarea nigripetala, and also recorded the highest values for relative coverage and frequency (Tab. S1 in supplementary material). Alcantarea trepida as the dominant species and codominant Pleroma cucullatum represented 67.44 % of IV in the Pedra do Elefante (Tab. S2 in supplementary material). In the two southern sampled areas, five species formed the dominant group; Melinis minutiflora, Cyperus pohlii, mosses, Pleroma heteromallum, Alcantarea extensa totaled 54 % (Tab. S3 in supplementary material) and V. plicata, M. minutiflora, Pteridium arachnoideum, Eremanthus crotonoides, Epidendrum secundum accounted for 53.19 % of this parameter (Tab. S4 in supplementary material), in Forno Grande and Pedra de Pontões, respectively (more details in the List S2 in supplementary material).

Floristic similarity

Floristically, the four inselbergs can be considered unique due to the low similarity (43 %) observed between the highest similarity inselbergs (Forno Grande and Pedra de Pontões), sites located in the south of Espírito Santo. Among northern inselbergs (Águia Branca and Pedra do Elefante) the similarity decreases to 30 %. When we compare inselbergs between regions the similarities decrease even more. Águia Branca presented similarity values of 16 % and 17 % with Forno Grande and Pedra de Pontões, respectively; and Pedra do Elefante presented similarity values of 22 % and 19 % with Forno Grande and Pedra de Pontões, respectively. From a total of 152 species, 110 species (72.3 %) occurred in only one of the four inselbergs studied, 30 species (19.7 %) in two, eight species (5.3 %) in three inselbergs and four species (Coleocephalocereus pluricostatus, Cyrtopodium glutiniferum, T. lhotzkiana and Vellozia candida) occurred in all four inselbergs, representing 2.6 % of the total. The CCC was 0.982.

Changes in community diversity and coverage

In terms of diversity measured by the Shannon Index (H’), the sampled areas in southern Espírito Santo presented the highest H' values and evenness (all results can be seen in Tab. 3).

We observed significant differences in species richness (Kruskal-Wallis test: Chi2 = 170.4, df = 3, p < 0.01, Fig. 2A), coverage (Chi2 = 120.5, df = 3, p < 0.001, Fig. 2B) and Shannon diversity index (Chi2 = 115.96, df = 3, p < 0.01, Fig. 2C) among sites when we analysed them at the sampling unit scale (Fig. 2). Species richness, cover, and Shannon index maintained similar patterns by region, with the highest values occurring in southern sites (Forno Grande and Pedra de Pontões). The Shannon-Wiener index showed a marked increase along the climatic gradient North-South, being significantly higher in southern sites (Fig. 2C). Conversely, Pielou evenness index showed a similar pattern between sites (Chi2 = 12.03, df = 3, p < 0.01, Fig. 2D).

Figure 2
Differences in plant coverage (A), species richness (B), Shannon index (C) and Pielou’s evenness index (D) along climatic gradient in the north-south axis, Espírito Santo, Brazil. Different letters indicate significant differences (Dunn test) among the inselbergs: AB - Águia Branca, PE - Pedra do Elefante, FG - Forno Grande and PP - Pedra de Pontões.

Phytogeography, endemism and threatened species

The distribution of inselberg flora showed that most species (37 %) were distributed exclusively in the Atlantic Forest phytogeographic domain. When we analyzed the distribution between domains, species shared exclusively with the Cerrado represented 17.2 %, with the Caatinga representing 4.76 % and Amazonia 3 %. The species occurring in the Atlantic Forest, Cerrado and Caatinga domains represented 12 %, adding the Amazon domain this value raises to 12.5 %.

Regarding the endemic species of Espírito Santo State, we found 13 species identified as endemic to rocky outcrops, and our survey also identified the presence of 24 species with occurrence exclusively on rocky outcrops. In relation to threatened species, we observed 21 species distributed among Red List categories (IUCN 2012IUCN. 2012. IUCN Red List Categories and Criteria: Version 3.1. 2nd. edn. Gland, Switzerland and Cambridge, UK, IUCN.): Vulnerable (33.3 %), Endangered (42.9 %), and Critically Endangered (23.8 %). When we analyzed by region the inselbergs of northern Espírito Santo had nine threatened species (69 %) identified as endemics of rocky outcrops while the southern inselbergs recorded four species (31%). The same patterns were observed for exclusive and threatened species: 21 spp. (84 %) and four spp. (16 %) were exclusive species; and 13 spp. (62 %) and 8 spp. (38 %) were threatened species for north and south inselbergs, respectively (more details in List S3 in supplementary material).

Discussion

This study demonstrated differences in floristic similarity, phytosociological structure, species richness, plant coverage, and Shannon diversity index among Brazilian inselberg with different elevational and climate conditions. Overall, the life-forms were similar among inselbergs, the number of endemic and/or threatened species was high, while the number of species shared with other phytogeographic domains was low.

The richest families and genera have been well represented in other studies of inselberg neotropical flora (França et al. 2005França F, Melo E, Santos AKA, et al. 2005. Estudos ecológicos e florísticos em ilhas de vegetação de um inselberg no semi-árido da Bahia, Brasil. Hoehnea 32: 93-101.; Alves et al. 2007Alves RJV, Cardin L, Kropf MS. 2007. Angiosperm disjunction “campos rupestres - restingas”: a re-evaluation. Acta Botanica Brasilica 21: 675-685. ; Caiafa & Silva 2007Caiafa AN, Silva AF. 2007. Structural analysis of the vegetation on a highland granitic rock outcrop in Southeast Brazil. Brazilian Journal of Botany 30: 657-664. ; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ; Ribeiro et al. 2007 Ribeiro KT, Medina BMO, Scarano FR. 2007. Species composition and biogeographic relations of the outcrop flora on the high plateau of Itatiaia, SE-Brazil. Brazilian Journal of Botany 30: 623-639. ; Esgario et al. 2009Esgario CP, Fontana AP, Silva AG. 2009. A flora vascular sobre rocha no Alto Misterioso, uma área prioritária para a conservação da Mata Atlântica no Espírito Santo, Sudeste do Brasil. Natureza Online 7: 80-91.; de Paula et al. 2017de Paula LFA, Mota NFO, Viana PL, Stehmann JR. 2017. Floristic and ecological characterization of habitat types on an inselberg in Minas Gerais, southeastern Brazil. Acta Botanica Brasilica 31: 199-211. ). These families and genera, common between regions and different inselbergs sites, probably are linked to habitat filtering, such as low nutrient, water availability, high radiation levels, and large temperature amplitude (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ). Thus, only taxons with specific adaptive traits, as morphological (i.e. caulescent rosette, succulence, and tank-forming) (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ), anatomical (i.e. pseudostems, adventitious roots, sclerophylly, pachycaulous and caudiciformous species) (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.), physiological (i.e. desiccation tolerance) (Kluge & Brulfert 2000Kluge M, Brulfert J. 2000. Ecophysiology of Vascular Plants on Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer Verlag . p. 143-170. ) and functional attributes associated with life history (i.e. life-form, resource acquisition, growth, reproduction, and dispersal) (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.) will be able to occur. The high floristic richness in the inselbergs studied is evident when we compared with other studies (i.e.Porembski et al. 1998Porembski S, Martinelli G, Onlemüller R, Barthlot W. 1998. Diversity and ecology of saxicolous vegetation mats on inselbergs in Brazilian Atlantic forest. Diversity and Distributions 4: 107-119. ; Meirelles 1999Meirelles ST, Pivello VR, Joly CA. 1999. The vegetation of granite rock outcrops in Rio de Janeiro, Brazil, and the need for its protection. Environmental Conservation 26: 10-20. ; Caiafa 2002Caiafa AN. 2002. Composição florística e estrutura da vegetação sobre um afloramento rochoso no Parque Estadual da Serra do Brigadeiro, MG. PhD Thesis, Universidade Federal de Viçosa, Viçosa.), and due to a large number of families with only one species, a characteristic pattern of places with high floristic richness (Ratter et al. 2003Ratter JA, Bridgewater S, Ribeiro JF. 2003. Analysis of the floristic composition of the Brazilian cerrado vegetation III: Comparison of the woody vegetation of 376 areas. Edinburg Journal of Botany 60: 57-109. ).

Regarding the phytosociological structure and physiognomy, we found a higher number of rare species than other studies focused on rocky outcrops (Meirelles 1996Meirelles ST. 1996. Estrutura da comunidade e características funcionais dos componentes da vegetação de um afloramento rochoso. PhD Thesis, Universidade Estadual de Campinas, São Paulo.; Conceição 2003Conceição AA. 2003. Ecologia da vegetação em afloramentos rochosos na Chapada Diamantina, Bahia, Brasil. PhD Thesis, Universidade de São Paulo, São Paulo.; Caiafa & Silva 2007Caiafa AN, Silva AF. 2007. Structural analysis of the vegetation on a highland granitic rock outcrop in Southeast Brazil. Brazilian Journal of Botany 30: 657-664. ), characteristic that demonstrates the oligarchism present in the rupicolous communities (Scarano 2002Scarano FR. 2002. Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Annals of Botany 90: 517-524. ). Therefore, Velloziaceae and Bromeliaceae families were observed to be extremely important in the inselbergs studied, due to the higher occurrence and relative importance of a single species from each family. This pattern was also found to be common to the rocky outcrops located in the Cerrado domain (Conceição & Giulietti 2002Conceição AA, Giulietti AM. 2002. Composição florística e aspectos estruturais de campo rupestre em dois platôs do Morro do Pai Inácio, Chapada Diamantina, Bahia, Brasil. Hoehnea 29: 37-48.) and the Atlantic Forest (Ribeiro & Medina 2002Ribeiro KT, Medina BMO. 2002. Estrutura, dinâmica e biogeografia das ilhas de vegetação sobre rocha do Planalto do Itatiaia, RJ. Boletim do Parque Nacional do Itatiaia 10: 18-21.), where Velloziaceae and Bromeliaceae families are most common mat-formers.

Some authors also report the high abundance (Conceição 2003Conceição AA. 2003. Ecologia da vegetação em afloramentos rochosos na Chapada Diamantina, Bahia, Brasil. PhD Thesis, Universidade de São Paulo, São Paulo.; Conceição & Pirani 2007Conceição AA, Pirani JR. 2007. Diversidade em quatro áreas de campos rupestres na Chapada Diamantina, Bahia, Brasil: espécies distintas, mas riquezas similares. Rodriguésia 58: 193-206. ) and adaptations (Kluge & Brulfert 2000Kluge M, Brulfert J. 2000. Ecophysiology of Vascular Plants on Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer Verlag . p. 143-170. ) of Velloziaceae family on rocky outcrops are related to poikilohydric adaptation to water stress (Dinakar et al. 2012Dinakar C, Djilianov D, Bartels D. 2012. Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Science 182: 29-41. ). Thus, during dry periods poikilohydric species tend to dehydrate, returning to a hydrated state with the rains, which is why they are also called “resurrection plants” (Porembski & Barthlott 2000Porembski S, Barthlott W. 2000. Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecology 151:19-28. ). This adaptation to water stress (desiccation tolerance) represents an important ecophysiological adaptation, influencing community structure and composition (Rietkerk & Koppel 2008Rietkerk M, Koppel J. 2008. Regular pattern formation in real ecosystems. Trends in Ecology & Evolution 23: 169-175. ; Meloni et al. 2017Meloni F, Granzotti CRF, Bautista S, Martinez AS. 2017. Scale dependence and patch size distribution: clarifying patch patterns in Mediterranean drylands. Ecosphere 8: 1-18. ), abundance Conceição 2003Conceição AA. 2003. Ecologia da vegetação em afloramentos rochosos na Chapada Diamantina, Bahia, Brasil. PhD Thesis, Universidade de São Paulo, São Paulo.; Conceição & Pirani 2007Conceição AA, Pirani JR. 2007. Diversidade em quatro áreas de campos rupestres na Chapada Diamantina, Bahia, Brasil: espécies distintas, mas riquezas similares. Rodriguésia 58: 193-206. ), diversity (Kluge & Brulfert 2000Kluge M, Brulfert J. 2000. Ecophysiology of Vascular Plants on Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer Verlag . p. 143-170. ) and phenology (Conceição 2003Conceição AA. 2003. Ecologia da vegetação em afloramentos rochosos na Chapada Diamantina, Bahia, Brasil. PhD Thesis, Universidade de São Paulo, São Paulo.).

Concerning the life-form spectrum, phanerophytes were the most commonly represented, as in other studies (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ; Caiafa & Silva 2005 Caiafa AN, Silva AF. 2005. Composição florística e espectro biológico de um campo de altitude no Parque Estadual da Serra do Brigadeiro, Minas Gerais - Brasil. Rodriguésia 56: 163-173. ; Ribeiro et al. 2007 Ribeiro KT, Medina BMO, Scarano FR. 2007. Species composition and biogeographic relations of the outcrop flora on the high plateau of Itatiaia, SE-Brazil. Brazilian Journal of Botany 30: 623-639. ; Gomes & Alves 2010Gomes P, Alves M. 2010. Floristic diversity of two crystalline rocky outcrops in the Brazilian northeast semi-arid region. Brazilian Journal of Botany 33: 661-676. ; de Paula et al. 2017de Paula LFA, Mota NFO, Viana PL, Stehmann JR. 2017. Floristic and ecological characterization of habitat types on an inselberg in Minas Gerais, southeastern Brazil. Acta Botanica Brasilica 31: 199-211. ). However, other studies have recorded chamaephytes (Conceição & Giulietti 2002Conceição AA, Giulietti AM. 2002. Composição florística e aspectos estruturais de campo rupestre em dois platôs do Morro do Pai Inácio, Chapada Diamantina, Bahia, Brasil. Hoehnea 29: 37-48.; Conceição et al. 2007Conceição AA, Giulietti AM, Meirelles ST. 2007. Ilhas de vegetação em afloramentos de quartzito-arenito no Morro do Pai Inácio, Chapada Diamantina, Bahia, Brasil. Acta Botanica Brasilica 21: 335-347. ) and therophytes (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.; Gomes & Sobral-Leite 2013Gomes P, Sobral-Leite M. 2013. Crystalline rock outcrops in the Atlantic Forest of northeastern Brazil: vascular flora, biological spectrum, and invasive species. Brazilian Journal of Botany 36: 111-123. ) to be predominant. The lack of a clear pattern between different geographic regions for inselberg life-form spectrum is still unknown (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ), e.g., therophytes are predominant on inselbergs in tropical Africa (Biedinger et al. 2000Biedinger N, Porembski S, Barthlott W. 2000. Vascular Plants on Inselbergs: Vegetative and Reproductive Strategies. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer Verlag. p. 117-140.), whereas in neotropical inselbergs phanerophytes, chamaephytes, and hemicryptophytes are more representative. Here, we assume that our results are related to microtopography variability, which can promote the accumulation of sediments in depressions, contributing to a greater establishment of phanerophytes and consequently their plant habits (mat-form and shrubs). Finally, life-form patterns will be better understood with a greater number of basic researches (Ribeiro et al. 2007 Ribeiro KT, Medina BMO, Scarano FR. 2007. Species composition and biogeographic relations of the outcrop flora on the high plateau of Itatiaia, SE-Brazil. Brazilian Journal of Botany 30: 623-639. ) associated with researches about ecological competition, biogeography (Safford & Martinelli 2000Safford HD, Martinelli G. 2000. Southeast Brazil. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 339-385. ) and changes in Pleistocene climate cycles (Yates et al. 2019Yates CJ, Robinson T, Wardell‐Johnson GW, et al. 2019. High species diversity and turnover in granite inselberg floras highlight the need for a conservation strategy protecting many outcrops. Ecology and Evolution 9: 7660-7675.).

A contrasting edaphoclimatic pattern was observed in the inselbergs studied, which topographic differences (altitude) and, especially, the geomorphological and microclimatic conditions (Gröger 2000Gröger A. 2000. Flora and vegetation of inselbergs of Venezuelan Guayana. In: Porembski S, Barthlott W. (eds.) Inselbergs: biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin, Heidelberg, Springer-Verlag. p. 291-314. ; Porembski 2007Porembski S. 2007. Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30: 579-586. ) of these outcrops can have a strong impact on plant community composition and structure. A recent study comparing Neotropical inselbergs demonstrated that altitude influence significantly the community composition and species richness and explain more variance than climate models (Pinto-Junior et al. 2020Pinto-Junior HV, Villa PM, Menezes LFT, Pereira MCA. 2020. Effect of climate and altitude on plant community composition and richness in Brazilian inselbergs. Journal of Mountain Science 17: 1931-1941. ). Plant coverage can be more sensitive than species diversity along an environmental gradient (He 2014He Y. 2014. The effect of precipitation on vegetation cover over three landscape units in a protected semi-arid grassland: temporal dynamics and suitable climatic index. Journal of Arid Environments 109: 74-82. ; Qin et al. 2018Qin X, Sun J, Wang X. 2018. Plant coverage is more sensitive than species diversity in indicating the dynamics of the above-ground biomass along a precipitation gradient on the Tibetan Plateau. Ecological Indicators 84: 507-514. ). Since plant coverage is the proportion of the community’s physical space occupied by plants (Ji et al. 2009Ji S, Geng Y, Li D, Wang G. 2009. Plant coverage is more important than species richness in enhancing aboveground biomass in a premature grassland, northern China. Agricuture, Ecosystems & Environment 129: 491-496. ), it is plausible that communities of plants with high coverage are more likely to use environmental resources efficiently than those with low coverage and thereby exhibit increased diversity (Ji et al. 2009Ji S, Geng Y, Li D, Wang G. 2009. Plant coverage is more important than species richness in enhancing aboveground biomass in a premature grassland, northern China. Agricuture, Ecosystems & Environment 129: 491-496. ; Sanaei et al. 2018Sanaei A, Chahouki MAZ, Ali A, Jafari M, Azarnivand H. 2018a. Abiotic and biotic drivers of aboveground biomass in semi-steppe rangelands. Science of The Total Environment 615: 895-905. a; bSanaei A, Ali A, Chahouki MAZ , Jafari M. 2018b. Plant coverage is a potential ecological indicator for species diversity and aboveground biomass in semi-steppe rangelands. Ecological Indicators 93: 256-266. ).

Our results showed that plant coverage was higher in sites with higher altitude and precipitation. Thus, the decrease in plant coverage might affect the sensitivity of dryland plant communities to environmental changes within the same vegetation type or within a given region (Vicente-Serrano et al. 2012Vicente-Serrano SM, Zouber A, Lasanta T, Pueyo Y. 2012. Dryness is accelerating degradation of vulnerable shrublands in semiarid Mediterranean environments. Ecological Monographs 82: 407-428. ). For example, a dominant trend toward decreased vegetation coverage is evident, mainly in summer and in areas affected by the most severe water stress conditions (i.e. low precipitation, higher evapotranspiration rates, and sun-exposed slopes), and sites with low plant coverage (< 30 %) are more sensitive to environmental changes than those with higher coverage (Vicente-Serrano et al. 2012Vicente-Serrano SM, Zouber A, Lasanta T, Pueyo Y. 2012. Dryness is accelerating degradation of vulnerable shrublands in semiarid Mediterranean environments. Ecological Monographs 82: 407-428. ).

We presume that, besides climate, fine-scale factors could also be determinant in plant coverage (i.e. soil depth and inclination) and consequently affect plant community composition and species richness. A previous study showed how patches size (which may be related to plant coverage) on a tropical inselberg has a strong influence on species composition, richness, and species abundance distribution (Villa et al. 2018Villa PM, Siqueira Cardinelli L, Magnago LF, et al. 2018a. Relación especie-área y distribución de la abundancia de especies en una comunidad vegetal de un inselberg tropical: efecto del tamaño de los parches. Revista de Biología Tropical 66: 937-951. a). Thus, one of challenges for future research is to assess the relationship between habitat types and plant coverage, and how these affect diversity patterns in Neotropical inselbergs.

We observed changes in species richness and composition, as well as contrasting differences in species shared between regions, probably due to factors acting on communities at a local and fine-scale (environmental filters), which may explain the high floristic dissimilarity between them. Perhaps, another important factor is the dispersal limitation of geographical distance, which can change markedly over relatively short distances (Schut et al., 2014Schut AGT, Wardell‐Johnson GW, Yates CJ, et al. 2014. Rapid characterization of vegetation structure to predict refugia and climate change impacts across a global biodiversity hotspot. PLOS ONE 9: e82778. doi: 10.1371/journal.pone.0082778
https://doi.org/10.1371/journal.pone.008...
). Island ecosystems such as inselbergs combine isolation with historical and environmental filtering and stochastic factors (Parmentier et al. 2005Parmentier I, Stévart T, Hardy OJ. 2005. The inselberg flora of Atlantic Central Africa. I. Determinants of species assemblages. Journal of Biogeography 32: 685-696.; Parmentier & Hardy 2009Parmentier I, Hardy OJ. 2009. The impact of ecological differentiation and dispersal limitation on species turnover and phylogenetic structure of inselberg’s plant communities. Ecography 32: 613-622. ). Therefore, different degrees of antiquity, occurrence in both tropical and temperate regions, overlaying a broad spectrum of sizes, can compensate the lower degree of geographical isolation and improving the effects of isolation (Porembski et al. 2000Porembski S, Seine R, Barthlott W. 2000b. Factors Controlling Species Richness of Inselbergs. In: Porembski S, Barthlott W. (eds.) Inselbergs - Biotic diversity of isolated rock outcrops in tropical and temperate regions . Berlin, Heidelberg, Springer-Verlag . p. 49-66. b). Thereby, as islands, inselbergs have an important phytogeographic contribution to regional diversity, due to their acting as a shelter for xeric vegetation of other domains, such as the Cerrado (Ratter et al. 1997Ratter JA, Ribeiro JF, Bridgewater S. 1997. The Brazilian cerrado vegetation and threats to its biodiversity. Annals of Botany 80: 223-230. ). In addition, our results showed a marked contrast in species shared with other phytogeographic domains, demonstrating a high degree of isolation, endemism, and species unique to Atlantic Forest inselbergs.

The high proportion of threatened species (12.5 %) and species exclusive to rocky outcrops (14.2 %) is surprising, due to the constant threats to this ecosystem, such as quarrying, plant overharvesting, weed invasion, fires, climate change, farming and tourism/sports/cultural activities (Porembski et al. 2016Porembski S, Silveira FAO, Fiedler PL, et al. 2016. Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodiversity and Conservation 25: 2827-2830. ). Another threat to inselbergs, and very common in the Espírito Santo State, is the so-called high altitude agriculture (Martinelli 2007Martinelli G. 2007. Mountain biodiversity in Brazil. Brazilian Journal of Botany 30: 587-597. ), as coffee and Eucalyptus plantations, which act as a gateway to invasive species. We observed high plant coverage of M. minutiflora (exotic and invasive) and P. arachnoideum (invasive) in the two most diverse communities of this study (Forno Grande and Pedra de Pontões). The presence of exotic and invasive species in inselberg communities is worrying because can lead to exclusion of native, endemic, and/or threatened species, resulting in loss of global biodiversity hotspot.

Our study indicated that communities have specific flora on each inselberg, giving an insular character to each community, as well as similar diversity patterns. Since floristic dissimilarity between these outcrops is so high (high β-diversity between outcrops), to protect the flora on inselbergs is a real challenge (de Paula et al. 2019de Paula LFA, Colmenares-Trejos SL, Negreiros D, et al. 2019. High plant taxonomic beta diversity and functional and phylogenetic convergence between two Neotropical inselbergs. Plant Ecology & Diversity 13: 61-73. ). Effective conservation strategies will need to focus on protecting multiple inselbergs across the entire climate gradient of the region (Yates et al. 2019Yates CJ, Robinson T, Wardell‐Johnson GW, et al. 2019. High species diversity and turnover in granite inselberg floras highlight the need for a conservation strategy protecting many outcrops. Ecology and Evolution 9: 7660-7675.), rather than a few inselbergs or those with higher species richness. In addition to ecological factors, the low genetic connectivity between isolated populations (e.g. Encholirium horridum) in Espírito Santo is already a strong indicator of the strategy of conserving multiple inselbergs (Hmeljevski et al. 2015Hmeljevski KV, Reis MS, Forzza RC. 2015. Patterns of gene flow in Encholirium horridum L.B.Sm., a monocarpic species of Bromeliaceae from Brazil. Journal of Heredity 106: 93-101.; 2017).

In this context, attention should be drawn to the “Monumento Natural dos Pontões Capixabas”, conservation unit with the highest number of inselbergs in the Atlantic Forest. More investments from the federal government are needed and most probably other conservation units in Espírito Santo State are highly recommended, as well as promoting the solution to several issues between local farmers and environmental agencies. We also propose other urgent conservation practices for inselbergs landscape, such as conservation initiatives “off-reserve” (Yates et al. 2019Yates CJ, Robinson T, Wardell‐Johnson GW, et al. 2019. High species diversity and turnover in granite inselberg floras highlight the need for a conservation strategy protecting many outcrops. Ecology and Evolution 9: 7660-7675.); local educational programs in conservation of biodiversity and water (Porembski et al. 2016Porembski S, Silveira FAO, Fiedler PL, et al. 2016. Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodiversity and Conservation 25: 2827-2830. ); to encourage sustainable tourism practices; creation of ex situ conservation programs for endangered species and the ones affected by mining (Porembski et al. 2016Porembski S, Silveira FAO, Fiedler PL, et al. 2016. Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodiversity and Conservation 25: 2827-2830. ); to guarantee the execution of mitigation actions by environmental agencies, and implementation of effective restoration strategies (Porembski et al. 2016Porembski S, Silveira FAO, Fiedler PL, et al. 2016. Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodiversity and Conservation 25: 2827-2830. ).

Conclusions

Our study demonstrated marked differences in plant community structure and diversity among local and regions scale, in addition to a specific flora on each inselberg, giving an insular character to each community. We believe this study and conservation strategies can contribute to the development of international legislation for the conservation of inselbergs at different scales. We highlight that the protection of many inselbergs is the most appropriate strategy for the conservation of this global biodiversity hotspot.

Acknowledgements

We thank the CAPES and CNPq for the scholarships of the first and second authors, respectively. This study is part of the master's thesis of the first author. We are grateful to PPGBT/UFES and IEMA for structure and research license. We thank IF Ribeiro, C Covre and WJ Souza for help with fieldwork. We are also grateful to DR Couto, RC Forzza, CN Fraga, LJC Kollmann and I Cordeiro for helped with plant identification.

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Publication Dates

  • Publication in this collection
    25 Jan 2021
  • Date of issue
    Oct-Dec 2020

History

  • Received
    04 Feb 2020
  • Accepted
    27 July 2020
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br