Abstract
Inselbergs are old outcrops, characterized by large expanses of open rocks and by distinct environmental filters. Many studies have been carried out on inselberg’s flora in the last decades. In contrast, vascular epiphytes received little attention compared to lithophytic groups. We aimed to investigate the role of inselbergs of the Espírito Santo as a refuge for epiphytic flora in Atlantic Forest in southeastern Brazil. In addition, we provide and discuss data on taxonomic representativeness, endemism, and threat status of the epiphyte species We used a combination of two online national databases of flora, species data collected by the authors and previously published studies. We record 266 species of vascular epiphytes (220 angiosperms; 43 ferns and three lycophytes), belonging to 89 genera and 18 families. Of these, three species (two orchids and one bromeliad) are restricted on Vellozia stems and represent an exceptional case of epiphyte-phorophyte specificity. For these species, we propose the term “specialist rock epiphytes”. The richest families were Orchidaceae, followed by Bromeliaceae and Polypodiaceae, while Vriesea, Acianthera, Epidendrum, Maxillaria, Peperomia, and Tillandsia represent the richest genera. The Espírito Santo inselbergs host endangered, endemic species, and a high number of species (77.0%) that are typical of the surrounding forest core of the Atlantic Forest, reinforcing the relevance of these xeric ecosystems as refuges for vascular epiphytes and that sometimes constitute the only chances of survival for native species epiphytes.
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References
Alves RJV, Kolbek J, Becker J (2008) Vascular epiphyte vegetation in rocky savannas of southeastern Brazil. Nord J Bot 26:101–117
Angelini C, Silliman BR (2014) Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree–epiphyte system. Ecology 95:185–196
Aximoff IA, Bovini MG, Fraga CN (2016) Vegetação em Afloramentos Rochosos Litorâneos Perturbados por Incêndios na Região Metropolitana Fluminense, Estado do Rio de Janeiro. Biodiversidade Brasileira 6:149–172
Barbosa DEF, Basilio GA, Pereira-Filho HRPm, Furtado SG, Menini Neto L (2022) Vascular epiphytes of Serra do Relógio: the surprising richness of the seasonal forest in the mountains of Minas Gerais. Southeastern Brazil Rodriguésia 73:e00492021
Barthlott W, Porembski S (2000) Why study inselbergs? In: Porembski S, Barthlott W (eds) Inselbergs—biotic diversity of isolated rock outcrops in tropical and temperate regions. Ecological studies. Springer, Berlin, pp 1–6
Benzing DH (1990) Vascular epiphytes. Cambridge University Press, Cambridge
BFG (2021) Brazilian Flora 2020: leveraging the power of a collaborative Flora do Brasil 2020. Taxon 71:178–198
Boelter CR, Dambros CS, Nascimento HEM, Zartman CE (2014) A tangled web in tropical tree-tops: effects of edaphic variation, neighbourhood phorophyte composition and bark characteristics on epipihytes in a central Amazonian Forest. J Veg Sci 25:1090–1099
Burke A (2002) Island–matrix relationships in Nama Karoo inselberg landscapes. Part I: do inselbergs provide a refuge for matrix species? Plant Ecol 160:79–90
Burns KC (2007) Network properties of an epiphyte metacommunity. J Ecol 95:1142–1151
Camp RJ, Knight RL (1998) Effects of rock climbing on cliff plant communities at Joshua Tree National Park, California. Conserv Biol 12:1302–1306
Carvalho G (2017) flora: tools for interacting with the Brazilian flora 2020. R package. 0.3.0. https://cran.r-project.org/web/packages/flora/index.html
Chiodi filho C (2009) Situação mundial e posição brasileira no setor de rochas ornamentais. São Paulo: ABIROCHAS. (Informe n. 18/2009)
CNCFlora (2020) Centro Nacional de Conservação da Flora. Disponível em http://cncflora.jbrj.gov.br/portal/
Condez TH, Tonini JFR, Pereira-Ribeiro J, Dubeux MJM (2021) On Atlantic Forest rock outcrops: the first record of Phyllopezus pollicaris (Spix, 1825) (Squamata, Phyllodactylidae) in the state of Espírito Santo, southeastern Brazil. Check List 17:1265–1276
Couto 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
Couto DR, Francisco TM, Manhães VC, Dias HM, Pereira MCA (2017) Floristic composition of a neotropical inselberg from the state of Espírito Santo, Brazil: a relevant area for conservation. Check List 13:1–12
Couto DR, Fontana AP, Rocha Neto AC, Gomes JML, Calazans LSB, Silva HL, Valadares RT, Saka MN, Siqueira GS, Lopes AS, Novelli FZ, Bergher IS, Fraga CN (2019a) Angiospermas monocotiledôneas ameaçadas de extinção no estado do Espírito Santo. In Fraga CN, Formigoni MH, Chaves FG (Orgs) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Santa Teresa, Instituto Nacional da Mata Atlântica, pp 164–191.
Couto DR, Francisco TM, Garbin ML, Dias HM, Pereira MCA, Menini Neto L, Pezzopane JEM (2019b) Surface roots as a new ecological zone for occurrence of vascular epiphytes: a case study on Pseudobombax trees on inselbergs. Plant Ecol 220:1071–1084
Couto DR, Dan ML, Aguiar WM, Braga JMA, Nascimento MT (2021) Floristic composition, structure and species-area relationships on a neotropical inselberg in southeastern Brazil. Rodriguésia 72:e00872020
Couto DR, Francisco TM, Trindade MS (2022a) Commensalistic epiphyte–phorophyte networks in woody vegetation of tropical inselbergs: patterns of organization and structure. Austral Ecol 47:911–927
Couto DR, Kessous IM, Neves B, Paixão-Souza B, Faria CG, Barfuss MHJ, Salgueiro F, Sa-Haiad B, Costa AF (2022b) Molecular phylogenetics and trait evolution in Stigmatodon (Bromeliaceae, Tillandsioideae), an endemic genus to Brazilian rocky outcrops. Syst Bot 47:347–362
Covre JMC, Couto DR, Dias HM, Zorzanelli JPF (2021) Vascular plants on inselberg landscapes in Espirito Santo state: bases for the creation of a protected area in southeastern Brazil. Acta Sci Biol Sci 43:54760
de Paula LFA, Negreiros D, Azevedo LO, Fernandes RL, Stehmann JR, Silveira FAO (2015) Functional ecology as a missing link for conservation of a resource-limited flora in the Atlantic forest. Biodivers Conserv 24:2239–2253
de Paula LFA, Forzza RC, Neri AV, Bueno M, Porembski S (2016) Sugar Loaf Land in south-eastern Brazil: a centre of diversity for mat-forming bromeliads on inselbergs. Bot J Linn 181:459–476
de Paula LFA, Colmenares-Trejos SL, Negreiros D, Rosado BH, de Mattos EA, de Bello F, Porembski S, Silveira FAO (2019) High plant taxonomic beta diversity and functional and phylogenetic convergence between two Neotropical inselbergs. Plant Ecol Divers 13:61–73
de Paula LFA, Azevedo LO, Mauad LP, Cardoso LJT, Braga JMA, Kollmann LJC, Fraga CN, Menini Neto L, Labiak PH, Mello-Silva R, Porembski S, Forzza RC (2020) Sugarloaf Land in south-eastern Brazil: a tropical hotspot of lowland inselberg plant diversity. Biodivers Data J 8:e53135
Dutra VF, Guarnier JC, Firmino AD, Tuler AC, Peixoto AL, Kameyama C, Saiter FZ, Barroso FG, Siqueira GS, Heiden G, Shimizu GH, Lima HC, Gomes JML, Trarbach J, Rossini J, Marinho LC, Simonelli M, Ribeiro M, Barros PHD, Santos PMLA, Goldenberg R, Cardoso WC (2019) Angiospermas eudicotiledôneas ameaçadas de extinção no estado do Espírito Santo. In Fraga CN, Formigoni MH, Chaves FG (Orgs) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Santa Teresa, Instituto Nacional da Mata Atlântica, pp 192–215.
Espírito Santo (2022) Decreto Estadual N° 5237-R, de 25 de novembro de 2022. Declara as espécies de fauna ameaçadas de extinção no Estado do Espirito Santo e dá outras providências. Diário Oficial Estadual, Vitória, Espírito, Edição 25.870. Disponível em: https://iema.es.gov.br/Media/iema/FAUNA/Decreto%205237-R_2022.pdf. Accessed 20 Feb 2023.
Flora e Funga do Brasil (2022) Jardim Botânico do Rio de Janeiro. Disponível em http://floradobrasil.jbrj.gov.br/.
Fraga CN (2004) Bulbophyllum boudetiana (Orchidaceae), a new species from the Brazilian Atlantic Forest, Espírito Santo. Novon 14:40–42
Fraga CN, Kollmann LJC (2010) Three new species of Pabstiella (Pleurothallidinae, Orchidaceae) from Brazilian Atlantic Forest. Harv Pap Bot 15:171–178
Fraga CN, Smidt EC (2004) Bulbophyllum arianeae (Orchidaceae), a new species from the Atlantic Forest of Espírito Santo. Brazil Harv Pap Bot 9:7–9
Fraga CN, Peixoto AL, Leite YLR, Santos ND, Oliveira JRPM, Sylvestre LS, Schwartsburd PB, Tuler AC, Freitas J, Lírio EJ, Couto DR, Dutra VF, Waichert C, Sobrinho TG, Hostim-Silva M, Ferreira RB, Bérnils RS, Costa LP, Chaves FG, Formigoni MH, Silva JP, Ribeiro RS, Reis JCL, Capellão RT, Lima RO, Saiter FZ, et al (2019) Lista da fauna e flora ameaçadas de extinção no estado do Espírito Santo. In: Fraga CN, Formigoni MH, Chaves FG (orgs) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Santa Teresa, Instituto Nacional da Mata Atlântica, pp 342–419
Francisco TM, Couto DR, Evans DM, Garbin ML, Ruiz-Miranda CR (2018) Structure and robustness of an epiphyte–phorophyte commensalistic network in a neotropical inselberg. Austral Ecol 43:903–914
Francisco TM, Couto DR, Garbin ML, Muylaert RL, Ruiz-Miranda CR (2019) Low modularity and specialization in a commensalistic epiphyte–phorophyte network in a tropical cloud forest. Biotropica 51:509–518
Freitas L, Salino A, Neto LM, Almeida TE, Mortara SR, Stehmann JR, Amorim AM, Guimaraes EF, Coelho MN, Zanin A, Forzza RC (2016) A comprehensive checklist of vascular epiphytes of the Atlantic Forest reveals outstanding endemic rates. Phytokeys 58:65–79
Gentry AH, Dodson CH (1987) Contribution of non-trees to species richness of a tropical rain forest. Biotropica 19:149–156
Gomes P, Alves M (2009) Floristic and vegetational aspects of an inselberg in the semi-arid region of northeast Brazil. Edinb J Bot 66:329–346
Guzmán-Jacob V, Weigelt P, Craven D, Zotz G, Krömer T, Kreft H (2021) Biovera-Epi: a new database on species diversity, community composition and leaf functional traits of vascular epiphytes along gradients of elevation and forest-use intensity in Mexico. Biodivers Data J 9:e71974
Hmeljevski KV, Reis MS, Forzza RC (2015) Patterns of gene flow in Encholirium horridum L.B.Sm., a monocarpic species of Bromeliaceae from Brazil. J Hered 106:93–101
IBGE (2017) Fitofisionomias. Base de dados em geociência. Disponível em https://www.ibge.gov.br/geociencias/downloads-geociencias.html. Accessed June 2018
IBGE (2022) Instituto Brasileiro de Geografia e Estatística. Disponível em. https://www.ibge.gov.br/cidades-e-estados/es.html. Accessed June 2022
IEMA (2016) Instituto Estadual de Meio Ambiente e Recursos Hídricos do Espírito Santo. GEOBASES—Tipos de solos. https://geobases.es.gov.br. Accessed March 2022
Kelly DL, O’Donovan G, Feehan J, Murphy S, Drangeid SO, Marcano-Berti L (2004) The epiphyte communities of a montane rain forest in the Andes of Venezuela: patterns in the dis- tribution of the flora. J Trop Ecol 20:643–666
Kersten RA (2010) Epífitos vasculares: Histórico, participação, taxonomia e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37:9–39
Kessous IM, Neves B, Couto DR, Paixão-Souza B, Pederneiras LC, Moura RL, Barfuss MHJ, Salgueiro F, Costa AF (2020) Historical biogeography of a Brazilian lineage of Tillandsioideae (Subtribe Vrieseinae, Bromeliaceae): the Paranaean Sea hypothesized as the main vicariant event. Bot J Linn 192:625–641
Krömer T, Kessler M, Gradstein SR (2007) Vertical stratification of vascular epiphytes in submontane and montane forest of the Bolivian Andes: the importance of the understory. Plant Ecol 189:261–278
Leme EMC, Kollmann LJC, Fontana AP (2009) Two new species from Pedra dos Pontões, an unexplored mountain in Espírito Santo, Brazil. J Bromel Soc 59:145–192
Leme EM, Fontana AP, Halbritter H (2010) Three new Pitcairnia species (Bromeliaceae) from the inselbergs of Espírito Santo, Brazil. Syst Bot 35:487–496
Mageski M, Ferreira RB, Zocca C, Teixeira RL, Rödder D (2014) The unusual occurrence of a population of Dendropsophus elegans (Anura: Hylidae) in an inselberg of southeastern Brazil. Herpetol Notes 7:363–365
Marcusso GM, Menini Neto L, Lombardi JA (2022a) Plants in the clouds: vascular epiphytes of Pedra Azul, a mountain top in Espírito Santo, Southeastern Brazil. Rodriguesia 73 Disponível em: http://hdl.handle.net/11449/234368
Marcusso MM, Menini Neto L, Lombardi JA (2022b) Augusto Ruschi Biological Reserve vascular epiphytes: a hotspot in the mountains of the Atlantic Forest of Southeastern Brazil. Phytotaxa 545:001–029
Martinelli G, Vieira CM, Gonzalez M, Leitman P, Piratininga A, Costa AF, Forzza RC (2008) Bromeliaceae da mata atlântica brasileira: Lista de espécies, distribuição e conservação. Rodriguésia 59:209–258
McMillan MA, Larson DW (2002) The effects of rock climbing on the vegetation of the Niagara Escarpment in Southern Ontario, Canada. Conserv Biol 16:389–398
Meirelles ST, Pivello VR, Joly CA (1999) The vegetation of granite rock outcrops in Rio de Janeiro, Brazil, and the need for its protection. Environ Conserv 1:10–20
Menini Neto L, van den Berg C, Forzza RC (2013) Taxonomic revision of Pseudolaelia Porto & Brade (Laeliinae, Orchidaceae). Acta Bot Bras 27:418–435
Michael DR, Cunningham RB, Lindenmayer DB (2008) A forgotten habitat? Granite inselbergs conserve reptile diversity in fragmented agricultural landscapes. J Appl Ecol 45:1742–1752
Moreira MM, Carrijo TT, Alves-Araújo A, Amorim AMA, Rapini A, da Silva AVS, Cosenza BAP, Lopes CR, Delgado CN, Kameyama C, Couto DR, Barbosa DEF, Monteiro D, Gonzaga DR, Dalcin EC, Guimarães EF, de Lírio EJ, Matos FB, Salimena FRG, Oliveira FA, Heiden G, Lanna JM, Baumgratz JF, Pastore JFB, Oliveira JRPM, Barcelos LB, Sylvestre LS, Freitas L, Giacomin LL, Pederneiras L, Meireles LD, Lohmann LG, Pereira LC, Silva LAE, Neto LM, Souza MC, Trovó M, Sobral MEG, Garbin ML, Gomes M, Morim MP, Mota MCA, Labiak PH, Viana PL, de Moraes PLR, Goldenberg R, Coelho RLG, Furtado SG, da Silva-Neto SJ, Flores TB, Dutra VF, Bueno VR, Forzza RC (2020) Using online databases to produce comprehensive accounts of the vascular plants from the Brazilian protected areas: the Parque Nacional do Itatiaia as a case study. Biodivers Data J 8:e50837
Myers N, Mittermeier R, Mittermeier C et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nadkarni NM (1984) Epiphyte biomass and nutrient capital of a neotropical elfin forest. Biotropica 16:249–256
Nadkarni NM, Matelson TJ (1989) Bird use of epiphyte re- sources in neotropical trees. Condor 91:891–907
Nieder J, Engwald S, Barthlott W (2000) Spatial distribution of vascular epiphytes (including Hemiepiphytes) in a Lowland Amazonian Rain Forest (Surumoni Crane Plot) of Southern Venezuela. Biotropica 32:385–396
Pessoa E, Alves M (2016) Taxonomic revision of Campylocentrum (Orchidaceae-Vandeae-Angraecinae): species with terete leaves. Syst Bot 41:700–713
Porembski S (2000) The invasibility of tropical granite outcrops (‘inselbergs’) by exotic weeds. J R Soc West Aust 83:131–137
Porembski S (2005) Epiphytic orchids on arborescent Velloziaceae and Cyperaceae: extremes of phorophyte specialisation. Nord J Bot 23:505–513
Porembski S (2007) Tropical inselbergs: habitat types, adapative strategies and diversity patterns. Rev Bras Bot 20:579–586
Porembski S, Barthlott W (2000a) Inselbergs—biotic diversity of isolated rock outcrops in tropical and temperate regions. Ecological Studies. Springer, Berlin
Porembski S, Barthlott W (2000b) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccationtolerant vascular plants. Plant Ecol 151:19–28
Porembski S, Martinelli G, Ohlemüller R, Barthlott W (1998) Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest. Divers Distrib 4:107–119
Porembski S, Silveira FAO, Fiedler PL et al (2016) Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodivers Conserv 25:2827–2830
QGIS Development Team (2015) QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
Quaresma AC, Jardim MAG (2014) Floristic composition and spatial distribution of vascular epiphytes in the restingas of Maracanã, Brazil. Acta Bot Bras 28:68–75
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. www.R-project.org/
Ramos FN et al (2019) Atlantic Epiphytes: a data set of vascular and non-vascular epiphyte plants and lichens from the Atlantic Forest. Ecology 100:2
Reitsma JM, Louis AM, Floret JJ (1992) Flore et végétation des inselbergs et dalles rocheuses première étude au Gabon. Bull Mus Natl Hist Nat 14:73–97
Rodrigues FG, Marulanda NF, Silva SR, Płachno BJ, Adamec L, Miranda VFO (2017) Phylogeny of the ‘orchid-like’ bladderworts (gen. Utricularia sect. Orchidioides and Iperua: Lentibulariaceae) with remarks on the stolon–tuber system. Ann Bot 120:709–723
Sarthou C, Villiers JF (1998) Epilithic plant communities on inselbergs in French Guiana. J Veg Sci 9:847–860
Scarano FR (2009) Plant communities at the periphery of the Atlantic rain forest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208
Silva JB, Sfair JC, dos Santos ND, Pôrto KC (2018) Different trait arrangements can blur the significance of ecological drivers of community assembly of mosses from rocky outcrops. Flora 238:43–45
Uribbe FP, Neves B, Jacques SSA, Costa AF (2020) Morphological variation in the Vriesea procera complex (Bromeliaceae, Tillandsioideae) in the Brazilian Atlantic Rainforest, with recognition of new taxa. Syst Bot 45:53–68
Valadares RT, Kollmann LJ, Sakuragui CM (2019) A new species of Anthurium (Araceae) with cordate leaves from southeastern Brazil. Novon 27:3–7
Zotz G (2016) Plants on plants—the biology of vascular epiphytes. Heidelberg, Berlin.
Zotz G, Bader M (2009) Epiphytic plants in a changing world: global change effects on vascular and non-vascular epiphytes. Progr Bot 70:147–170
Zotz G, Weigelt P, Kessler M, Kreft H, Taylor A (2021) EpiList 1.0: a global checklist of vascular epiphytes. Ecology 102:e03326
Acknowledgements
This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Programa de Capacitação Institucional (PCI) of the Ministério da Ciência, Tecnologia e Inovações (MCTI) within the Instituto Nacional da Mata Atlântica (INMA): Grants (TMF #300906/2022-6 and DRC #301141/2022-3). CNF is grateful to Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro for their respective grants (FAPERJ, Programa Jovem Cientista do Nosso Estado, Grant No. 201.280/2022) and CNPq (Edital Universal, Grant No. 422191/2021-3). The authors thank Instituto Nacional da Mata Atlântica (INMA) and Instituto de Pesquisas Jardim Botânico do Rio de Janeiro (JBRJ) for their support. Special thanks to Joelcio Freitas for the vector illustration and the reviewers and editor for their suggestions.
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TMF contributed to conceptualization, data acquisition, data curation, methodology, investigation, writing—original draft, writing-review, and editing. DRC contributed to conceptualization, data curation, methodology, investigation, writing-review. CNF and MMM contributed to the methodology, investigation, and writing-review. APF data availability.
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Table S1. List of vascular epiphytes on inselbergs in the Espírito Santo State, Brazil. Data indicates whether we obtain species data from online databases (DB - JABOT-JBRJ, www.jbrj.gov.br/jabot e Reflora http://reflora.jbrj.gov.br/ reflora / herbarioVirtual /), through collections of authors (C) or published articles (R). The voucher or reference indicates the vouchers with the respective herbarium abbreviation or the article reference (see references at the end of the table). In addition to the number of specimens per species, single records, and old records were obtained from online databases. Life form, substrate type, origin and endemism to Brazil, phytogeographic domain, endemic to the Atlantic Forest, vegetation types, occur on inselberg followed the Flora e Funga do Brasil 2022 (http://floradobrasil.jbrj.gov.br). The threatened category for Brazil followed the National Flora Conservation Center (http://www.cncflora.jbrj.gov.br/portal); for the threat category for the state of Espírito Santo (Fraga et al., 2019): DD = Deficient Data, NT = Near Threatened, VU = Vulnerable, CR = Critically Endangered, EN = Endangered, LC = Least Concern, NE = not evaluated. No information = indicates that data is missing for that species. Supplementary file1 (XLSX 46 kb)
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Francisco, T.M., Couto, D.R., Moreira, M.M. et al. Inselbergs from Brazilian Atlantic Forest: high biodiversity refuges of vascular epiphytes from Espírito Santo. Biodivers Conserv 32, 2561–2584 (2023). https://doi.org/10.1007/s10531-023-02618-7
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DOI: https://doi.org/10.1007/s10531-023-02618-7