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Eriocaulaceae in the Brazilian Amazon and the use of Species Distribution Modelling in its conservation

Abstract

Following a survey in herbaria in Brazil and abroad, complemented by a survey of the literature and searches of biodiversity data, 66 taxa of Eriocaulaceae have been identified in the Brazilian Amazon, as defined by the states of Acre, Amapá, Amazonas, Pará, Rondônia and Roraima. Six genera of Eriocaulaceae were found in the Amazon with the following taxon numbers: Comanthera (3 taxa), Eriocaulon (10), Paepalanthus (15), Rondonanthus (2), Syngonanthus (35) and Tonina (1). Of this total, 25 taxa present distributions in the states of the Amazon and other Brazilian states (considered as widely distributed) and the remaining 41 taxa are restricted to the Amazon Rainforest biome. The distribution data for 31 species were used for Species Distribution Modelling, due to the low number of occurrence points reported for the other taxa, 17 of those are known from a single location. The overlap of these models indicates areas from Amapá, Amazonas, Pará and Roraima where modelled species are most likely to occur. These data can further contribute to the location of new populations of species of Eriocaulaceae. New detection of Eriocaulaceae species can assist in filling the gaps on their geographic distribution and ecology, contributing to the protection or restoration of priority areas set aside for their conservation.

Key words:
geographical distribution; species conservation; potential geographic distribution modeling

Resumo

Com base em espécimes de herbários do Brasil e exterior, complementado pela literatura pertinente e buscas em sites de biodiversidade, foram identificados 66 táxons de Eriocaulaceae para a Amazônia brasileira, definida pelos estados do Acre, Amapá, Amazonas, Pará, Rondônia e Roraima. Seis gêneros de Eriocaulaceae foram encontrados na Amazônia com os seguintes números de táxons: Comanthera (3 táxons), Eriocaulon (10), Paepalanthus (15), Rondonanthus (2), Syngonanthus (35) e Tonina (1). Desse total, 25 táxons foram considerados como de distribuição ampla e os restantes 41 táxons são restritos ao bioma Floresta Amazônica. Os dados de distribuição para apenas 31 táxons foram utilizados para Modelagem de Distribuição de Espécies, devido ao baixo número de pontos de ocorrência reportados para os outros táxons, 17 dos quais conhecidos de uma só localidade. A sobreposição desses modelos mostrou áreas do Amapá, Amazonas, Pará e Roraima como tendo maior probabilidade de ocorrência para as espécies modeladas. Os dados obtidos permitirão a localização de novas populações das espécies de Eriocaulaceae. Novas detecções das espécies de Eriocaulaceae podem ajudar a preencher as lacunas sobre sua distribuição geográfica e ecologia, contribuindo para a proteção ou restauração de áreas prioritárias para sua conservação.

Palavras-chave:
distribuição geográfica; conservação de espécies; modelagem de distribuição geográfica potencial

Introduction

The Eriocaulaceae is a pantropical family of around 1,400 species placed in 10 genera (Giulietti et al. 2012aGiulietti, A.M.; Andrade, M.J.G.; Scatena, V.L.; Trovó, M.; Coan, A.I.; Sano, P.T.; Santos, F.A.R.; Borges, R.L. & van den Berg, C. 2012a. Molecular phylogeny, morphology and their implications for the taxonomy of Eriocaulaceae. Rodriguésia 63: 1-19.). Molecular studies corroborated by morphological data show two well-supported lineages: Eriocaulaceae subf. Eriocauloideae, which includes the genera Eriocaulon, with about 500 species and a pantropical and subtropical distribution, and Mesanthemum, with about 15 species restricted to Africa. Eriocaulaceae subf. Paepalanthoideae includes the remaining eight genera, which, apart from the North American Lachnocaulon, occur mainly in South America (Andrade et al. 2010Andrade, M.J.G.; Giulietti, A.M.; Rapini, A.; Queiroz, L.P.; Conceição, A.S.; Almeida, P.R.M. & Van den Berg, C. 2010. A comprehensive molecular phylogenetic analysis of Eriocaulaceae: evidence from nuclear (ITS) and plastid (trnH-psbA and trnL-trnF) DNA sequences. Taxon 59: 379-388.; Giulietti et al. 2012aGiulietti, A.M.; Andrade, M.J.G.; Scatena, V.L.; Trovó, M.; Coan, A.I.; Sano, P.T.; Santos, F.A.R.; Borges, R.L. & van den Berg, C. 2012a. Molecular phylogeny, morphology and their implications for the taxonomy of Eriocaulaceae. Rodriguésia 63: 1-19.). Giulietti & Hensold (1990)Giulietti, A.M. & Hensold, N. 1990. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasílica 4: 133-158. have commented that the Paepalanthoideae have two centers of diversity, the main being in the mountains of Central Brazil, especially in the Espinhaço range in Minas Gerais and Bahia, and the other in the mountains of Northern South America, especially in Venezuela, where eighty eight species in six genera occur (Hensold 1999Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58.). In Paepalanthoideae the main genera are Paepalanthus with 500 species (Trovó et al. 2013Trovó, M.; Andrade, M.J.G.; Sano, P.T.; Ribeiro, P.L. & van den Berg, C. 2013. Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae). Botanical Journal of the Linnean Society 171: 225-243.) and Syngonanthus with 150 species (Echternacht et al. 2014Echternacht, L.; Sano, P.T.; Bonillo, C.; Cruaud, C.; Couloux, A. & Dubuisson, J. 2014. Phylogeny and taxonomy of Syngonanthus and Comanthera (Eriocaulaceae): Evidence from expanded sampling. Taxon 63: 47-63.), which occur predominantly in South America, but with some species in North and Central America, the Caribbean and also in Africa. The monotypic genus Tonina has a Neotropical distribution, and the remainder: Actinocephalus, Comanthera, Leiothrix, and Rondonanthus are restrict to South America, this last being restricted to the very North of the continent (Ruhland 1903Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294.; Giulietti & Hensold 1990Giulietti, A.M. & Hensold, N. 1990. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasílica 4: 133-158.; Hensold 1999Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58.; Parra et al. 2010Parra, L.R.; Giulietti, A.M.; Andrade, M.J.G. & van den Berg, C. 2010. Reestablishment and a new circumscription of Comanthera (Eriocaulaceae). Taxon 59: 1135-1146.; Andrade et al. 2010Andrade, M.J.G.; Giulietti, A.M.; Rapini, A.; Queiroz, L.P.; Conceição, A.S.; Almeida, P.R.M. & Van den Berg, C. 2010. A comprehensive molecular phylogenetic analysis of Eriocaulaceae: evidence from nuclear (ITS) and plastid (trnH-psbA and trnL-trnF) DNA sequences. Taxon 59: 379-388.; Giulietti et al. 2012aGiulietti, A.M.; Andrade, M.J.G.; Scatena, V.L.; Trovó, M.; Coan, A.I.; Sano, P.T.; Santos, F.A.R.; Borges, R.L. & van den Berg, C. 2012a. Molecular phylogeny, morphology and their implications for the taxonomy of Eriocaulaceae. Rodriguésia 63: 1-19.; Trovó et al. 2013Trovó, M.; Andrade, M.J.G.; Sano, P.T.; Ribeiro, P.L. & van den Berg, C. 2013. Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae). Botanical Journal of the Linnean Society 171: 225-243.; Echternacht et al. 2014Echternacht, L.; Trovó, M.; Oliveira, C.T. & Pirani, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206: 782-791.).

In Brazil, there are 625 species in eight genera, occurring in all regions and biomes of the country (BFG 2015BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.). The main center of diversity of the family in the country is situated in the upper parts of the mountains that compose the Espinhaço range in the states of Minas Gerais and Bahia, associated with "campo rupestre" vegetation. The other species occur in lakes and fresh water lagoons, especially species of Eriocaulon, in other mountains not associated with the Espinhaço range, in "cerrado" vegetation and in coastal dunes ("restingas") (Giulietti & Pirani 1988Giulietti, N.; Giulietti, A.M.; Pirani, J.R. & Menezes, N.L. 1988. Estudos em sempre-vivas: importância econômica do extrativismo em Minas Gerais, Brasil. Acta Botânica Brasílica 1: 179-193.; Giulietti & Hensold 1990Giulietti, A.M. & Hensold, N. 1990. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasílica 4: 133-158.; Giulietti et al. 1997Giulietti, A.M.; Pirani, J.R. & Harley, R.M. 1997. Espinhaço Range Region, Eastern Brazil. In: Davis, S.D.; Heywood, V.H.; Herrera-MacBryde, O.; Volla-Lobos, J. & Hamilton, A.C. (eds). Centres of plant diversity. Vol. 3. Americas. WWF/IUCN, Washington. Pp. 397-404.; Echternacht et al. 2011Echternacht, L.; Trovó, M.; Oliveira, C.T. & Pirani, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206: 782-791.; Hensold et al. 2012Hensold, N.; Oliveira, A. & Giulietti, A.M. 2012. Syngonanthus restingensis (Eriocaulaceae): A remarkable new species endemic to Brazilian costal shrublands. Phytotaxa 40: 1-11.; Trovó et al. 2015Trovó, M.; Echternacht, L.; Costa, F.N.; Giulietti, A.M. & Sano, P.T. 2015. Nomenclatural and taxonomic notes on Eriocaulaceae from the Atlantic Forest, Brazil. Phytotaxa 205: 249-258.).

The Eriocaulaceae possess very small unisexual flowers with white scarious sepals and petals, which are grouped in compact monoecious capitula at the end of a scape. The scapes, with the capitula and flowers, when detached from the rest of the plant, continue to appear living, from which the popular names of "everlasting plants", or in Brazil "sempre-vivas", originate. Because of their beauty, the scapes and capitula are collected and sold as decoration in the house, and has resulted in an intensive extractive industry (Giulietti et al. 1988Giulietti, A.M. & Pirani, J.R. 1988. Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In: Vanzolini, P.E. & Heyer, W.R. (eds.). Proceedings of a workshop on neotropical distribution patterns. Academia Brasileira de Ciências, Rio de Janeiro. Pp. 39-69., 1996Giulietti, A.M.; Wanderley, M.G.L.; Longhi-Wagner, H.M.; Pirani, J.R. & Parra, L.R. 1996. Estudos em "sempre-vivas": taxonomia com ênfase nas espécies de Minas Gerais, Brasil. Acta Botânica Brasílica 10: 329-377.; Oliveira et al. 2015Oliveira, M.N.S.; Dias, B.A.; Andrade, G.C.; Tanaka, M.K.; Ávila, R.G. & Silva, L.C. 2015. Harvest times of Comanthera elegans, a worldwide traded Brazilian species of everlasting flower: implications on seed production, germination, and on species management. Brazilian Journal of Botany 38: 795-808. DOI 10.1007/s40415-015-0179-1.
https://doi.org/10.1007/s40415-015-0179-...
).

Also, a large proportion of the species of Eriocaulaceae are considered to be rare or endemic to a small area. Giulietti et al. (2009)Giulietti, A.M.; Andrade, M.J.G.; Trovó, M. & Sano, P.T. 2009. Catálogo de plantas raras do Brasil: Eriocaulaceae. In: Giulietti, A.M. et al. (eds.). Plantas raras do Brasil. Conservação Internacional, Belo Horizonte. Pp. 166-180. lists 109 species of the family as rare, nine of which are restricted to the Amazon Rainforest biome. The high level of endemism in the Eriocaulaceae is often mentioned, especially for the Espinhaço range, where most studies have been concentrated (Giulietti & Hensold 1990Giulietti, A.M. & Hensold, N. 1990. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasílica 4: 133-158.; Giulietti et al. 1997Giulietti, A.M.; Pirani, J.R. & Harley, R.M. 1997. Espinhaço Range Region, Eastern Brazil. In: Davis, S.D.; Heywood, V.H.; Herrera-MacBryde, O.; Volla-Lobos, J. & Hamilton, A.C. (eds). Centres of plant diversity. Vol. 3. Americas. WWF/IUCN, Washington. Pp. 397-404.). Echternacht et al. (2011)Echternacht, L.; Trovó, M.; Oliveira, C.T. & Pirani, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206: 782-791. lists 77 species of the genera Actinocephalus, Comanthera e Paepalanthus for the Espinhaço range of Minas Gerais. This high level of endemism of Eriocaulaceae in the Campo Rupestre, certainly contributes to the position that this vegetation type supports the highest level of endemism in the country: There are 1,951 endemic species, 39.6% of the 4,928 listed (BFG 2015BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.). In the "Livro Vermelho da Flora do Brasil" 12 species of Eriocaulaceae are listed as threatened, and are defined particularly by the high level of endemism, and for two species on account of their commercial importance in the trade of Everlasting Flowers (Martinelli & Moraes 2013Martinelli, G. & Moraes, M.A. 2013. Livro vermelho da flora do Brasil. Andrea Jakobsson: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro. 1100p.). These same species were listed in Decree no. 443 of the Ministry of the Environment of Brazil, which included no Eriocaulaceae from Amazonia (MMA 2014MMA. 2014. Portaria nº 443 de 17 de dezembro de 2014. Lista nacional oficial das espécies da Flora ameaçadas de extinção. Diário Oficial da União, Seção 1, nº 245. Pp. 110-121.). Regarding projects involving the conservation of Eriocaulaceae, an Action Plan for the Conservation of "Sempre Vivas" is currently being developed, initially focusing on 20 species from the Espinhaço range, of which five are of concern, due to the high level of commercial extraction, and 15 due to their very local endemism (MMA 2015MMA. 2015. Sumário executivo do Plano Nacional para conservação das sempre-vivas. ICMBio, Brasília. 8p.).

BFG (2015)BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113. notes that, of the five other Brazilian biomes, the Amazon Rainforest biome showed the least increase in the number of new species since the original "Catálogo das Espécies do Brasil" (Forzza et al. 2010Forzza, R.G.; Baumgratz, J.F.; Costa, A.; Hopkins, M.; Leitman, P.M.; Lohmann, L.G.; Martinelli, G.; Morin, M.P.; Coelho, M.A.N.; Peixoto, A.L.; Pirani, J.R.; Queiroz, L.P.; Stehmann, R.; Walter, B.M.T. & Zappi, D. 2010. As Angiospermas do Brasil. In: Forzza et al. (org.). Catálogo de plantas e fungos do Brasil. Vol. 1. Instituto de Pesquisas Jardim Botânico, Rio de Janeiro. Pp. 78-88.) was published, and which showed a decrease in the number of endemic species in the biome. The authors consider that this situation is due to the relatively very small number of scientific plant collections made in the Northern Region of Brazil, in relation to its size.

Our knowledge of the Eriocaulaceae of Amazônia is extremely fragmented and based on very few published works, of which could be mentioned: Koernicke (1863)Koernicke, F. 1863. Eriocaulaceae. In: Martius, C.F.P.; Eichler, A.G. & Urban, N.I. (eds.). Flora Brasiliensis. Typographia Regia, Monachii, Munchen. Vol. 3, pars 1, pp. 271-508., who mentions 17 species for the Brazilian Amazon, based primarily on collections made by Spruce and Schomburgk. Ruhland (1903)Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294. who increased this number to 20, mostly including species of Paepalanthus ser. Leptocephali Ruhland and of Syngonanthus. The most important work published on the Eriocaulaceae of Amazonia was by Hensold (1999)Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58., who accounts for 88 species for the Flora of the Venezuelan Guayana. Also, various species were described by Moldenke and Herzog from the region (see Results and Appendix 1).

More recently, studies of Amazonian species involving both phylogenetic and taxonomic research are now under way, and these continue lines of research already published: Hensold & Giulietti (1991)Hensold, N. & Giulietti, A.M. 1991. Revision and redefinition of the genus Rondonanthus Herzog (Eriocaulaceae). Annals of Missouri Botanical Garden 78: 441-459. for Rondonanthus, Parra et al. (2010)Parra, L.R.; Giulietti, A.M.; Andrade, M.J.G. & van den Berg, C. 2010. Reestablishment and a new circumscription of Comanthera (Eriocaulaceae). Taxon 59: 1135-1146. for Comanthera, Giulietti et al. (2012b)Giulietti, A.M.; Hensold, N.; Parra, L.R.; Andrade, M.J.G.; van den Berg, C.; Harley, R.M. 2012b. The synonymization of Philodice with Syngonanthus (Eriocaulaceae). Phytotaxa 60: 50-56. for Philodice, Echternacht et al. (2014Echternacht, L.; Sano, P.T.; Bonillo, C.; Cruaud, C.; Couloux, A. & Dubuisson, J. 2014. Phylogeny and taxonomy of Syngonanthus and Comanthera (Eriocaulaceae): Evidence from expanded sampling. Taxon 63: 47-63., 2015)Echternacht, L.; Sano, P. & Dubuisson, J. 2015. Taxonomic study of Comanthera subg. Thysanocephalus (Eriocaulaceae). Systematic Botany 40: 136-150. and Watanabe (2015)Watanabe, M.C. 2015. Sistemática de Syngonanthus. Tese de Doutorado. Instituto de Biociências da Universidade de São Paulo, São Paulo. 182p. for Comanthera and Syngonanthus.

At the start of 2005, the first author received a request from Dr. Ricardo Secco, then the Curator of the Herbarium at the Museu Paraense Emilio Goeldi (MG), to determine the large number of still unidentified specimens of Eriocaulaceae collected in Amazonia, which were held there. This material was sent directly to the Royal Botanic Gardens of Kew (K), where the first author was carrying out her post-doctoral studies, engaged in a study of type material of Eriocaulaceae held in European herbaria. The process of identifying the specimens from MG herbarium was the start of a study of Amazonian material with a view to producing a list of Eriocaulaceae of the region. In spite of the relatively large number of species, which were recorded from the Amazon Rainforest biome of Brazil, a large proportion of these was poorly known and restricted to the type material or very few other collections.

The objectives of the present work are to present a preliminary list of Eriocaulaceae species occurring in the Brazilian Amazon and to determine potential occurrence areas using known distributional data of Amazonian Eriocaulaceae using Species Distribution Modelling. The results obtained and the discussion presented in this paper should make possible the discovery and collection of new populations of rare or little-known species. This will contribute to the filling of gaps in our understanding of the family in the Amazon biome and provide data to aid their conservation.

Material and Methods

Elaboration of the list of Eriocaulaceae species

As referred in the Introduction, the curator of the herbarium MG sent a loan of the material to K for studies of Giulietti, A.M. in 2005. The initial examination of these specimens, followed by subsequent visits to herbaria in Rio de Janeiro (RB) and Manaus (INPA), demonstrated the rich taxonomic diversity of the Eriocaulaceae in the Amazon region, with a species number much greater than the 20 species originally proposed by Ruhland (1903)Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294.. From there arose an interest to develop a list of species from the Brazilian Amazon, as a first step towards a better understanding of their diversity (Appendix 1).

The six core Amazonian states: Acre, Amapá, Amazonas, Pará, Roraima, and Rondônia, were selected to provide data for the elaboration of the list of taxa (Appendix 1). The North of Mato Grosso state and the North-western of Tocantins, in spite of now being form of the Amazon Rainforest biome, were not included in this study, because of our very sparse understanding of the Eriocaulaceae of these areas. Visits were also made to study the collections of a number of Brazilian and foreign herbaria, especially for type material: B, BM, E, F, HBG, K, INPA, M, MG, NY e RB (acronyms according Thiers [continuously updated]). These data were complemented with those from the taxonomic bibliography of Koernicke (1863)Koernicke, F. 1863. Eriocaulaceae. In: Martius, C.F.P.; Eichler, A.G. & Urban, N.I. (eds.). Flora Brasiliensis. Typographia Regia, Monachii, Munchen. Vol. 3, pars 1, pp. 271-508., Ruhland (1903)Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294. e Hensold (1999)Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58., as well as those of Rondonanthus (Hensold & Giulietti 1991Hensold, N. & Giulietti, A.M. 1991. Revision and redefinition of the genus Rondonanthus Herzog (Eriocaulaceae). Annals of Missouri Botanical Garden 78: 441-459.), Philodice (Giulietti et al. 2012bGiulietti, A.M.; Hensold, N.; Parra, L.R.; Andrade, M.J.G.; van den Berg, C.; Harley, R.M. 2012b. The synonymization of Philodice with Syngonanthus (Eriocaulaceae). Phytotaxa 60: 50-56.), Comanthera subg. Comanthera (Parra & Giulietti 2010Parra, L.R.; Giulietti, A.M.; Andrade, M.J.G. & van den Berg, C. 2010. Reestablishment and a new circumscription of Comanthera (Eriocaulaceae). Taxon 59: 1135-1146.) and Comanthera subg. Thysanocephalus (Echternacht et al. 2015Echternacht, L.; Sano, P. & Dubuisson, J. 2015. Taxonomic study of Comanthera subg. Thysanocephalus (Eriocaulaceae). Systematic Botany 40: 136-150.). Special attention was paid to the protologues of the species, principally those described by Herzog and Moldenke, referred in the Appendix 1.

Development of the Species Distribution Modelling

We used Species Distribution Modeling (SDM) (Franklin 2009Franklin, J. 2009. Mapping species distribution. Spatial inference and prediction. Cambridge, New York. 320p.) to detect potential occurrence areas of Eriocaulaceae. We selected the eight least correlated environmental variables from an original dataset of 20 variables (following Aguirre-Gutierrez 2013Aguirre-Gutierrez, J.; Carvalheiro, L.G.; Polce, C.; Loon, E.E.; Raes, N.; Reemer, M. & Biesmeijer, J.C. 2013. Fit-for-purpose: species distribution model performance depends on evaluation criteria. Dutch hoverflies as a case study. PlosOne 8: e63708.; Giannini et al. 2015Giannini, T.C.; Tambosi, L.R.; Acosta, A.L.; Jaffé, R.; Saraiva, A.M.; Imperatriz-Fonseca, V.L. & Metzger, J.P. 2015. Safeguarding ecosystem services: a methodological framework to buffer the joint effect of habitat configuration and climate change. PLoS ONE 10: e0129225.) provided by Worldclim website (Hijmans et al. 2005Hijmans, R.; Cameron, S.; Parra, J.; Jones, P. & Jarvis, A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.), which were based on temperature and precipitation averages obtained from meteorological stations around the world for the last 50 years. The eight variables (with a resolution of 5 arc-minute) were Annual Mean Temperature; Isothermality; Max Temperature of Warmest Month; Min Temperature of Coldest Month; Mean Temperature of Driest Quarter; Precipitation of Wettest Month; Precipitation of Wettest Quarter; and Precipitation of Coldest Quarter. Altitude was excluded from the remained eight variables due to its high correlation. We did not include any other variable besides climate (such as soil, for example) due to the lack of such information with high resolution covering all the studied area.

The Maximum Entropy algorithm (Maxent - Philipps et al. 2006Phillips, S.J.; Anderson, R.P. & Schapire, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259.) was used to perform SDM because it is especially useful for species that contain low known number of occurrence points and also, because it requires only presence points (and not absence points, as the case of other algorithms) (Wisz et al. 2008Wisz, M.S.; Hijmans, R.J.; Li, J.; Peterson, A.T.; Graham, C.H. & Guisan, A. 2008. Predicting species distributions working group. Effects of sample size on the performance of species distribution models. Diversity and Distributions 14: 763-773.). We used 20% of occurrence points (randomly sampled by the Maxent program) to perform an internal test aiming to estimate the Area Under Receiver-Operating Curve (AUC). AUC varies from 0-1 and values near to 1 indicate good accuracy (Stockwell et al. 2002Stockwell, D. & Peterson, A.T. 2002. Effects of sample size on accuracy of species distribution models. Ecological Modelling 148: 1-13.).

Aiming to define the complete known species geographical distribution, especially of those occurring outside the Amazon Rainforest biome, we used the data included in the Appendix 1 and complemented it with species occurrence data from speciesLink biodiversity data provider (<http://splink.cria.org.br>). From the 66 selected species of Eriocaulaceae, only 31 presented more than 10 occurrence points and were modelled. Draft maps of each species were firstly plotted on the speciesLink website and visually checked, aiming to detect erroneous data (such as points occurring on water bodies) and, after that, the data were corrected using ArcGIS (Esri Inc.).

At the end of SDM procedure, all the obtained models for each species (31 models) were normalized, that is, we standardized the scale of probability of each model to vary from 0-1. After that, all the obtained models (31 models) were united in one final model. We did this aiming to show the areas with the highest probability of occurrence of the studied species. This final model was normalized again, but we rescaled it to vary from 0-100% of occurrence probability. For all these procedures, we used the 'raster' package (Hijmans 2014Hijmans, R. 2014. Raster: geographic data analysis and modeling, 2.2-31. CRAN repository. Available at <https://cran.r-project.org/web/packages/raster/index.html>. Access on June 2015.
https://cran.r-project.org/web/packages/...
) for R (R Development Core Team. 2011R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN: 3-900051-07-0. Available at <http://www.R-project.org/>. Access on June 2015.
http://www.R-project.org/...
). Finally, we plotted this final model as a map using ArcGIS (Esri Inc.).

Results

For Eriocaulaceae 66 taxa were identified from the Brazilian Amazon Rainforest biome, including the following genera, with their respective number of species and varieties: Comanthera (3 species), Eriocaulon (10 species), Paepalanthus (13 species and 2 varieties), Rondonanthus (2 species), Syngonanthus (30 species and 5 varieties) and Tonina (1 species) (Tab. 1, Appendix 1). Of the six taxa at varietal level, five were described from the Brazilian Amazon: Paepalanthus piresi var. piresi, P. piresi var. villosus, Syngonanthus bracteosus var. scrupulosus, S. egleri var. egleri and S. egleri var. pomboensis. Of special interest is the presence of Rondonanthus only in this region of Brazil, and the proportionally high representation of species of Eriocaulon with 17.5% of the 57 reported from all Brazil and Syngonanthus with 37% of the 94 species reported (BFG 2015BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.).

From the total of taxa surveyed, 24 species and two varieties were found to have a wide geographical distribution within the six Amazonian states in Brazil, elsewhere in other Brazilian biomes, and also outside the country. All the 42 remaining taxa have distributions restricted to the Amazon Rainforest biome, with 21 species and one variety presenting a wider distribution within the biome, extending to other areas outside Brazil. The remaining 14 species and four varieties are each restricted to a single locality within the biome (Tab. 1; Appendix 1).

Table 1
List of Eriocaulaceae species recorded for the Brazilian Amazon Rainforest Biome (states of Acre, Amazonas, Amapá, Pará, Roraima and Rondônia).
Tabela 1
Lista de espécies de Eriocaulaceae registradas para o Bioma Floresta Amazônica Brasileira (estados do Acre, Amazonas, Amapá, Pará, Roraima e Rondônia).

It was possible to generate potential distribution models for only 30 species and one variety, of which 19 species and one variety are of wide distribution, and 12 species are restricted to the Amazon Rainforest biome (Appendix 2). All models presented an AUC of over 0.8, suggesting results of a good quality.

We draw attention to the following models as examples which display a pattern of wide distribution, represented by Comanthera xeranthemoides, Syngonanthus gracilis, and S. nitens (Fig. 1) and those models with a distribution pattern restricted to the Amazonian Forest, represented by Eriocaulon tenuifolium, Paepalanthus fasciculatus and Syngonanthus fenestratus (Fig. 2).

Figure 1
Three examples of Eriocaulaceae species whose occurrence points and Species Distribution Modelling show wide distribution in Brazil. Warmer colors (near red) indicates high occurrence probability.
Figura 1
Três exemplos de espécies de Eriocaulaceae cujos pontos de ocorrência e Modelagem de Distribuição de Espécies mostram uma ampla distribuição geográfica no Brasil. Cores mais quentes (perto do vermelho) indicam alta probabilidade de ocorrência.
Figure 2
Three examples of Eriocaulaceae species whose occurrence points and Species Distribution Modelling show distribution restricted to the Amazon Rainforest biome. Warmer colors (near red) indicates high occurrence probability.
Figura 2
Três exemplos de espécies de Eriocaulaceae cujos pontos de ocorrência e Modelagem de Distribuição de Espécies mostram uma distribuição geográfica restrita ao bioma Floresta Amazônica. Cores mais quentes (perto do vermelho) indicam alta probabilidade de ocorrência.

Bringing together all the models obtained, two distinct groups were encountered for the geographical distribution of species of Eriocaulaceae of the Brazilian Amazon: 1 - including species of wide distribution, some with a northern limit in Central America and reach along the coastal dunes ("restingas") via Maranhão and North-east Brazil as far as the southern limits of the tropics. 2 - Including the species whose occurrence is more concentrated in Amazonia, extending westwards as far as Mato Grosso state, or to the South-east via Tocantins and Goiás states. The modelling pattern of all species confirms that the major probability of species occurrence is within the Amazonian Rainforest and Cerrado biomes (Fig. 3). In Amazonia, the state of Pará (principally eastern and south-eastern areas) and the eastern region of Amapá, Amazonas and Roraima states are pinpointed. In the Cerrado, the South of Pará, northern of Mato Grosso and Rondônia, Tocantins, Goiás and some areas in Maranhão state are highlighted.

Figure 3
Occurrence probability based on the potential distribution of 31 species of Eriocaulaceae, using Species Distribution Modelling and Geographic Information Systems - A. Oiapoque; B. Barcelos; C. Novo Ariapuanã; D. Manaus; E. São Gabriel da Cachoeira; F. Santa Isabel do Rio Negro; G. Manicorá; H. Humaitá; I. Borba; J. Novo Progresso; K. Parauapebas; L. Oriximiná; M. Santarém; N. Vigia; O. Monte Roraima. Warmer colors (near red) indicates high occurrence probability.
Figura 3
Probabilidade de ocorrência baseada na distribuição potencial de 31 espécies de Eriocaulaceae, utilizando-se Modelagem de Distribuição Geográfica e Sistemas de Informação Geográfica - A. Oiapoque; B. Barcelos; C. Novo Ariapuanã; D. Manaus; E. São Gabriel da Cachoeira; F. Santa Isabel do Rio Negro; G. Manicorá; H. Humaitá; I. Borba; J. Novo Progresso; K. Parauapebas; L. Oriximiná; M. Santarém; N. Vigia; O. Monte Roraima. Cores mais quentes (perto do vermelho) indicam alta probabilidade de ocorrência.

When superimposing the potential areas obtained with the 31 species used by SDM, it can be seen there is a high level of agreement (Fig. 3). Areas with the largest number of species occurring in the same localities or areas very close, and arranged by state, are:

  1. Amapá. Rio Oiapoque region, 12 species, all widely distributed.

  2. Amazonas. Barcelos: Serra do Aracá with 11 species, including Paepalanthus gleasonii only known from this locality. Novo Ariapuanã: Rio Aripuanã with 10 species, including Syngonanthus bracteosus var. scrupulosus only known from this locality. Manaus and surroundings: with nine species including Syngonanthus heteropeploides only known from this locality. São Gabriel da Cachoeira: Rio Issana with four species, including Syngonanthus amazonicus only known from this locality. Santa Isabel do Rio Negro: Pico da Neblina with three species, including Paepalanthus major and P. sulcatus only known from this locality. Other areas which should be mentioned are: Manicorá: Rio Cururu with 10 species, on the borders of Rondônia; Humaitá with seven species, and Borba with five species.

  3. Pará. Novo Progresso: Serra do Cachimbo with 11 species, with three taxa, Paepalanthus piresii var. piresii, Syngonanthus cachimboensis and S. sickii, only known from this locality. Parauapebas: Serra dos Carajás with eight species, including Eriocaulon carajasense, Paepalanthus fasciculoides and Syngonanthus diversifolius, only known from this locality. Oriximiná: Rio Mapuera with six species, including Paepalanthus singularis, only known from this locality. There are also important localities for the collection of Eriocaulaceae in the Santarém area, Alto Tapajós with 11 species, and Vigia with five species.

  4. Roraima. The most important site here is the Parima Mountains with Mount Roraima presenting two species, including the only locality known for a record of Rondonanthus roraimensis.

  5. Rondônia. All the species recorded from this state have wide distribution and are associated with cerrado areas, which extend into the neighboring areas of Mato Grosso, Tocantins, Goiás, some areas in Maranhão and also outside Brazil in Bolívia.

Discussion

The supposedly low occurrence of Eriocaulaceae species in Northern Brazil is primarily a reflection of the small number of species mentioned from the area in the classic works, such as the Flora Brasiliensis (Koernicke 1863Koernicke, F. 1863. Eriocaulaceae. In: Martius, C.F.P.; Eichler, A.G. & Urban, N.I. (eds.). Flora Brasiliensis. Typographia Regia, Monachii, Munchen. Vol. 3, pars 1, pp. 271-508.) and in Das Pflanzenreich (Ruhland 1903Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294.). Only 20 taxa are mentioned for the area in these works, and some of the names mentioned therein are now in the synonymy of other accepted names. Additionally, with the exception of the few taxa described from the 19th and early 20th century collections of Spruce and Ule, the remainder were described from collections made outside Brazil, especially Guiana, Jamaica, and Surinam.

In the early 1900s, there was an increase in collections from the Amazon, notably by Luetzelburg, which were deposited in the Munich Herbarium, and described particularly by Herzog. In the 1960-1990s, Prance and collaborators collected many Eriocaulaceae especially from the state of Amazonas, and Paulo Cavalcanti and Murça Pires in the state of Pará, which provided material for the description of many new taxa by H. Moldenke. In the same period, there was an active development of floristic studies in the Guayana Highlands of Venezuela, which provided many new taxa of Eriocaulaceae, and species of other families from the region.

Steyermark (1982)Steyermark, J. 1982. Relationship of some Venezuelan forest refuges with lowland tropical floras. In: Prance, G.T. (ed.). Biological diversification in the tropics. Colombia University Press, New York. Pp. 182-221. considered the Venezuelan Highland as a refugee area, and the geological formations as well the present-day physiography as the main factors responsible for the region's plant distribution and endemism. Hensold (1999)Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58. recorded seven genera and 88 species of Eriocaulaceae from the Venezuelan mountains. The author included Philodice but it was placed in synonymy of Syngonanthus (Giulietti et al. 2012bGiulietti, A.M.; Hensold, N.; Parra, L.R.; Andrade, M.J.G.; van den Berg, C.; Harley, R.M. 2012b. The synonymization of Philodice with Syngonanthus (Eriocaulaceae). Phytotaxa 60: 50-56.). Also four species referred as Syngonanthus, actually are included in Comanthera. Comparing the species lists from the Venezuelan Highland and the Brazilian Amazon Rainforest biome, all the genera and 42 species have been recorded from both areas. It is now known that 100% of the species of Comanthera, Rondonanthus and Tonina are common to the two areas, while in Paepalanthus the percentage is 84.6%, for Syngonanthus 57.1% and for Eriocaulon it is 50% of species. Most of these species, common to the two areas, have wide distributions, while a few other merit mention: Paepalanthus fasciculoides occurs in Venezuela only on the "Cerro Cotorra" in Bolivar state, at an altitude of 600 m, and in Brazil only on the Serra dos Carajás, in Pará state, Brazil, at about 800 m altitude. In this latter locality, from where the type material originated (Hensold 1991Hensold, N. 1991. Revisionary studies in the Eriocaulaceae of Venezuela. Annals of the Missouri Botanical Garden 78: 441-459., 1999Hensold, N. 1999. Eriocaulaceae. In: Steyermark, J.A.; Berry, P.; Yatskievych, K. & Holst, B. Flora of Venezuelan Guyana. Vol. 5. Eriocaulaceae- Lentibulariaceae. Missouri Botanical Garden, Saint Louis. Pp. 1-58.), populations with numerous individuals occur, varying from caulescent to acaulous plants. Paepalanthus major was described from material collected on the Serra da Neblina, in Amazonas state, Brazil, and also occurs on Auyán-tepui in Venezuela (Hensold 1991Hensold, N. 1991. Revisionary studies in the Eriocaulaceae of Venezuela. Annals of the Missouri Botanical Garden 78: 441-459.).

An analysis of the general distribution of Eriocaulaceae taxa show that a relatively small number of species are widely distributed (ca. 39,4%) while the majority (60.6%) show a restricted distribution within the Amazon Rainforest biome. Of these, 22.3% are known only from a single locality. This arrangement of species as differentiated distribution patterns appears to be common in different areas, as much in the Tropics as in temperate regions (Henrys et al. 2015Henrys, P.A.; Smart, S.M.; Rowe, E.C.; Jarvis, S.G.; Fang, Z.; Evans, C.D.; Emmett, B.A. & Butler, A. 2015. Niche models for British plants and lichens obtained using an ensemble approach. New Journal of Botany 5: 89-100.; Smart et al. 2015Smart, S.M.; Jarvis, S.; Walker, K.J.; Henrys, P.A.; Pescott, O.L. & Marrs, R.H. 2015. Common plants as indicators of habitat suitability for rare plants; quantifying the strength of the association between threatened plants and their neighbors. New Journal of Botany 5: 72-88.).

In Amazonia, three species show a wider and disjunct pantropical distribution pattern in the tropics. These are Eriocaulon cinereum and E. setaceum, which are aquatic plants occurring in Asia, Africa and tropical America. The third species, Paepalanthus lamarckii, occurs in West Africa and in the Americas from Central America to South-east Brazil (Ruhland 1903Ruhland, W. 1903. Eriocaulaceae. In: Engler, A. (ed.). Das Pflanzenreich. Vol. IV. Engelmann, Leipzig. Pp. 301-294.; Giulietti & Hensold 1990Giulietti, A.M. & Hensold, N. 1990. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasílica 4: 133-158.).

Species with a neotropical distribution can be cited: Paepalanthus bifidus, P. tortilis, P. subtilis, Syngonanthus caulescens, S. davidsei, S. gracilis, S. nitens and Tonina fluviatilis. All these species are composed of populations of annual plants, occurring in damp, sandy soils. P. bifidus e T. fluviatilis occur in low-lying areas, associated especially with the forests in eastern Amazonia or in the coastal restingas, where they extend both northwards and south, as far as South-east Brazil. The remaining species are particularly associated with mountain ranges, reaching southwards to Minas Gerais or São Paulo, and in the case of S. caulescens as far as Argentina.

The species Comanthera xeranthemoides, Eriocaulon gibbosum, E. humboldtii, Paepalanthus chiquitensis, Syngonanthus densiflorus and S. longipes occur mainly in savanna areas (Cerrado Biome), extending mostly towards the Central-Western of Brazil and also parts of Bolivia and Colombia.

Populations of Eriocaulaceae can be found in diverse areas of the Amazon Rainforest biome and in Cerrado Biome, although some areas are characterized by the higher number of species, as was noted in the Results. These areas can be tentatively classified into four groups, based on the Brazilian relief classification (Ross 1990Ross, J.L.S. 1990. Uma nova proposta de classificação do relevo do Brasil. Revista do Departamento de Geografia USP 4: 25-39.) and their structures and forms (Ross 2013Ross, J.L.S. 2013. Brazilian Relief: structures and forms. Revista do Departamento de Geografia USP 25: 42-58.).

Areas included in the "Sedimentary Plateau" of the eastern (Oriental) Amazon River. This plateau results from Tertiary and Mesozoic sediments and reaches altitudes up to 300 to 400 m. The main areas include Manaus (AM), Santarém and Vigia (PA). The annual Eriocaulaceae species from those areas occur especially along river margins and littoral restingas.

Areas included in the "Sedimentary Plateau" of the western (Occidental) Amazon River. This plateau reaches a maximum altitude of 200 m, being formed from Tertiary and Quaternary sediments of the Solimões Formation. The main areas include São Gabriel da Cachoeira, Borba and Oriximiná (AM). The annual Eriocaulaceae species from those areas occur especially along river margins.

Areas included in the "Crystalline Plateau" named "Residuais Norte-Amazônico" (Northern Amazonian Residuals). They are a series of disjunct mountains of the Pre-cambrian origin, which form part of the Guiana Shield. They extend from Amapá state up to the northern part of Amazonas state, with altitudes in general between 600-1000 m, and include the highest Brazilian plateaus, such as Pico da Neblina (Serra do Imeri, Amazonas) with 2,995 m and Monte Roraima (Serra do Pacaraima, Roraima) with 2,734 m. The substrates are of sandstone, quartzite, granite or volcanic inclusions and the main vegetation is "Campo Rupestre". The main areas include Oiapoque, Barcelos, Santa Isabel do Rio Negro, Monte Roraima, and other mountain areas nearby, where the perennial Eriocaulaceae species usually occur.

Areas included in the "Crystalline Plateau" named "Residuais Sul-Amazônico" (Southern Amazonian Residuals). This covers a large area from southern Pará to Rondônia state. In the West, in areas such as Nova Aripoanã, Manicorá, Humaitá and Novo Progresso, there are formations with an ancient sedimentary cap, characterized by flat tops with altitudes up to 1000 m, covered with a cerrado vegetation. In the East, also occur residual reliefs up to 900 m altitude, originating from ancient volcanism, associated with intrusions and folding, as can be found in the Serra dos Carajás in Parauapebas. In these mountains, there are an intermingling of different types of forest formation, and the upper parts is normally occupied with "Campo Rupestre" overlying ironstone, locally recognized as the "vegetation of canga". The flora on the canga on this area is rich and diversified with about 600 species of plants and there are annual and perennial Eriocaulaceae species.

The study presented here will aid the collection of new species and new populations of Eriocaulaceae. It should also prove useful in the search for species of other families of Angiosperms, which display a similar distribution and share areas in Amazonia with the same edaphic and climatic features. The species thus collected will provide the bases for further taxonomic, phylogenetic and biogeographical studies, which will help our understanding of the vegetation history of the Amazon basin. This is a region of immense changes in the past, which suffered the impact of the rise of the Andes, the change in the direction of the waters of the Amazon River eastward, as well as major climatic changes during and since the Quaternary, as referred by Fiaschi & Pirani (2009)Fiaschi, P. & Pirani, J.R. 2009. Review of plant biogeographic studies in Brazil. Journal of Systematic and Evolution 47: 477-496.. The results of species modelling will also be a key contribution towards the future selection of priority areas of conservation/restoration within the region.

Acknowledgment

We would like to express our gratitude to the curators and staff for allowing us to access the collections of Eriocaulaceae from Amazonia, especially D. Simpson curator of the K herbarium and R. Secco and P. Viana curators of the MG herbarium. Giulietti, A.M. would like to acknowledge the financial support and "Bolsa de Produtividade Sênior" from CNPq. We also thank Dr. Vera Lucia Imperatriz Fonseca from ITVDS for support during the research development.

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Publication Dates

  • Publication in this collection
    Oct-Dec 2016

History

  • Received
    01 Jan 2016
  • Accepted
    26 Apr 2016
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