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Species richness and distribution of bryophytes within different phytophysiognomies in the Chapada Diamantina region of Brazil

Abstract

The Chapada Diamantina ecoregion is within the caatinga (shrublands) biome of Brazil. Environmental factors determine the phytophysiognomies that distinguish the ecoregion from the surrounding areas. This study aimed to investigate the distribution of bryophyte flora in this ecoregion, by phytophysiognomy and elevational zone. Analyzing specimens we collected from five municipalities in the region, together with specimens (previously collected from the region) in herbaria, we identified 400 taxa. The phytophysiognomies that presented the highest species richness and the greatest numbers of exclusive taxa were forests and campos rupestres (dry, rocky grasslands), which respectively accounted for 51% and 40% of the taxa, compared with only 5% and 4%, respectively, for the caatinga and cerrado (savanna). Species richness and the numbers of exclusive taxa were highest in the lower and upper montane zones. There was a predominance of neotropical taxa and a significant number of disjunct species found in Brazil and in the Andes region. We conclude that the Chapada Diamantina region is an important center of bryophyte diversity, harboring not only a great number of species overall but also a considerable number of species exclusive to the region, primarily in forests and campos rupestres at elevations above 800 m.

Mosses; liverworts; forests; campos rupestres; elevational zonation


ARTICLES

Species richness and distribution of bryophytes within different phytophysiognomies in the Chapada Diamantina region of Brazil1 1 Based on the Doctoral thesis of the first Author

Emilia de Brito ValenteI,* * Author for correspondence: ebvalente@gmail.com , Kátia Cavalcanti PôrtoII; Cid José Passos BastosIII

IUniversidade Estadual do Sudoeste da Bahia, Departamento de Ciências Naturais, Vitória da Conquista, BA, Brazil

IIUniversidade Federal de Pernambuco, Departamento de Botânica, Centro de Ciências Biológicas, Programa de Pós Graduação em Biologia Vegetal, Recife, PE, Brazil

IIIUniversidade Federal da Bahia, Instituto de Biologia, Departamento de Botânica, Campus de Ondina, Salvador, BA, Brazil

ABSTRACT

The Chapada Diamantina ecoregion is within the caatinga (shrublands) biome of Brazil. Environmental factors determine the phytophysiognomies that distinguish the ecoregion from the surrounding areas. This study aimed to investigate the distribution of bryophyte flora in this ecoregion, by phytophysiognomy and elevational zone. Analyzing specimens we collected from five municipalities in the region, together with specimens (previously collected from the region) in herbaria, we identified 400 taxa. The phytophysiognomies that presented the highest species richness and the greatest numbers of exclusive taxa were forests and campos rupestres (dry, rocky grasslands), which respectively accounted for 51% and 40% of the taxa, compared with only 5% and 4%, respectively, for the caatinga and cerrado (savanna). Species richness and the numbers of exclusive taxa were highest in the lower and upper montane zones. There was a predominance of neotropical taxa and a significant number of disjunct species found in Brazil and in the Andes region. We conclude that the Chapada Diamantina region is an important center of bryophyte diversity, harboring not only a great number of species overall but also a considerable number of species exclusive to the region, primarily in forests and campos rupestres at elevations above 800 m.

Key words: Mosses, liverworts, forests, campos rupestres, elevational zonation

Introduction

The ecoregion of Chapada Diamantina, in the state of Bahia, Brazil, is one of the centers of plant diversity of the Americas (Giulietti et al. 1997). It is located within the caatinga (shrublands) biome (IBGE 2004), constituting one of its eight ecoregions (Velloso et al. 2002), and is entirely surrounded by the ecoregion of the Sertaneja Meridional Depression, the borders between the two being defined primarily by changes in physical aspects such as elevation, geological formation, climate, rainfall, topography and soil type (Rocha et al. 2005), which result in a mosaic of vegetation in the former (Giulietti & Pirani 1988). According to the Brazilian Ministry of the Environment (MMA 2005), the vegetation in the Chapada Diamantina ecoregion comprises campos rupestres (dry, rocky grasslands), semi-deciduous montane forests, montane rain forests, cerrado (savanna) and caatinga.

Bryophytes, which represent the object of this study, are strongly influenced by external factors, particularly water and light, and differences in their physiognomy, composition, richness and abundance are evident among different vegetation formations and habitats (Mägdefrau, 1982). Numerous studies have indicated that bryophyte composition varies along an elevational gradient, showing greater diversity with increasing elevation (Van Reenen & Gradstein, 1983, 1984; Frahm, 1990; Frahm & Gradstein, 1991; Gradstein 1995; Kessler, 2000; Andrew et al., 2003; Ah-peng, 2007), this feature is also a consequence of high bryophyte sensitivity to climatic conditions.

In Brazil, the elevational zonation of bryophytes has been examined in two separate studies, both conducted in the Atlantic Forest within the state of Rio de Janeiro (Costa & Lima, 2005; Santos & Costa, 2010a). In both studies, the authors found that there is a variation in bryophyte flora composition along an elevational gradient, and that species richness, the number of exclusive taxa and the number of endemic taxa are highest in montane forests (sensu Veloso et al. 1991), followed by upper montane formations, lower montane formations and lowlands (sensu Veloso et al. 1991).

As previously mentioned, the vegetation formations found in the Chapada Diamantina ecoregion include forests, campos rupestres,cerrado and caatinga. Among those, the highest bryophyte species richness and abundance is found in the forests. Therefore, in Brazil as a whole, systematic floristic studies of bryophytes have most often been conducted in forests, including those in the states of Rio de Janeiro (Costa 1999; Costa & Lima 2005; Molinaro & Costa 2001; Santos & Costa 2010a, 2010b), Espírito Santo (Costa & Silva 2003; Yano 2005), São Paulo (Visnadi 2005; Visnadi & Vital 2000; Peralta & Yano 2005), Pernambuco (Pôrto 1990, 1992; Germano & Pôrto 1996; Campelo & Pôrto 2007; Alvarenga & Pôrto 2007), Alagoas (Silva & Pôrto 2009) and Bahia (Valente & Pôrto 2006; Bastos & Valente 2008; Bastos & Vilas Bôas-Bastos 2008; Vilas Bôas-Bastos & Bastos 2008; Valente et al. 2009). Studies of bryophytes in the cerrado have been conducted in the states of São Paulo (Egunyomi & Vital 1984; Visnadi 2004), Bahia (Vilas Bôas-Bastos & Bastos 1998) and Piauí (Castro et al. 2002), as well as in the Federal District of Brasília (Câmara & Costa 2006; Câmara 2008a, 2008b). In the campos rupestres, bryophytes have been studied in the state of Minas Gerais-in the Serra do Cipó (Yano 1987), Serra da Piedade (Yano & Carvalho 1995) and Grão Mogol (Yano & Peralta 2009)-and in the state of Bahia, specifically within the Chapada Diamantina ecoregion (Harley 1995; Bastos et al. 1998a, 2000). Studies of bryophytes in the caatinga have been conducted in the states of Pernambuco (Pôrto et al. 1994) and Bahia (Bastos et al. 1998b).

The fact that there have been few studies of bryophytes in the Chapada Diamantina ecoregion is most likely attributable to the small number of researchers in this field of botany and the enormity of the region. The first contribution to knowledge of the bryophyte flora of this region was a species list compiled by Harley (1995), which included 28 species of liverworts and 37 species of mosses identified in the Pico das Almas region, near the municipality of Rio de Contas. Later, Bastos et al. (1998a) reported 27 species of mosses, collected in campos rupestres and in gallery forests near the town of Lençóis. In addition, Bastos et al. (2000) identified 65 species belonging to the divisions Bryophyta (n = 41) and Marchantiophyta (n = 24) in campos rupestres. Those authors stated that the majority of the bryophyte taxa surveyed in the Chapada Diamantina ecoregion have not been found elsewhere in the state of Bahia. A recently published Checklist of Bryophytes in the Chapada Diamantina region (Valente et al. 2011) lists 414 taxa, including various new records for the state of Bahia, for northeastern Brazil and for Brazil as a whole.

Considering the physical and climatic conditions, the phytophysiognomies within the Chapada Diamantina ecoregion and the bryophyte response to these conditions, this study aimed to investigate the distribution of the bryophyte flora in the phytophysiognomies and elevational zones in this ecoregion within the caatinga biome of Brazil.

Material and methods

Study area

The Chapada Diamantina ecoregion is 400 km in length and covers an area of 50,000 km2, representing approximately 9% of the State of Bahia. Elevations in the region range from 400 m to 2033 m, making it the highest point in northeastern Brazil (MMA 2005). According to Nolasco et al. (2008), the average monthly temperature can be as low as 0ºC in the winter (June through August) or as high as 30ºC in the summer (in December and January). The rainy season is from November to April, with maximum rainfall in December (139 mm), and the dry season is from May to October, with minimum rainfall in August (20 mm). The average monthly rainfall exceeds 100 mm during the rainy season, compared with approximately 35 mm during the dry season. The average annual rainfall ranges from 600 mm to 1100 mm (Agritempo 2010). Geologically, the Chapada Diamantina ecoregion consists of quartzite and sandstone outcrops, and there are a number of rivers in the region (Rocha et al. 2005).

The type of phytophysiognomy that is the most characteristic of the Chapada Diamantina ecoregion is campos rupestres, which typically occur at elevations above 900 m and are characterized mainly by rocky outcrops associated with herb-shrub areas, typically on quartzite soils, the predominant species belonging to the families Velloziaceae, Melastomataceae, Eriocaulaceae, Xyridaceae and Orchidaceae (Conceição et al. 2005). Forest types, including semideciduous forest, premontane rain forest and montane rain forest, typically to the east of the main mountain range, also occur on plateaus (plateau forests), along the banks of rivers (riparian forests) and between large rocky cliffs (cove forests) (Funch et al. 2005; Funch 2008; Queiroz et al. 2008). Throughout the region, cerrado occurs at elevations of 900-1200 m and is interspersed with campos rupestres, where rocky outcrops and shallow soils appear more frequently. At lower elevations, the cerrado is replaced by various forms of dry forest or caatinga (Harley et al. 2005). Caatinga, or phytophysiognomies associated with it, cover the greatest area in the region, albeit quite diverse in its physiognomy, floristic composition and community structure, and is found mainly to the west of the main mountain range (Queiroz et al. 2005).

Sampling

Specimens were collected during 11 field campaigns conducted between 2007 and 2009 in the Chapada Diamantina ecoregion, in the municipalities of Morro do Chapéu and Miguel Calmon (located in the north of the region) Lençóis and Palmeiras (in the center); and Piatã and Abaíra (in the south). The municipalities were selected considering the preexisting knowledge about the diversity of other plant groups (MMA 2005) and the presence of the target phytophysiognomies and elevational zones. In each municipality, three to six sites were surveyed. The areas were walked for approximately seven hours, and the sampling effort was given by stabilization of the species accumulation curve. The samples collected were deposited in the Herbarium of the Estate University of Feira de Santana (code, HUEFS), with duplicates in the Herbarium of the Federal University of Pernambuco (code, UFP). We employed traditional methods of collection and preservation, as described by Yano (1989b).

The sampling sites were located across five ecologically protected areas (Chapada Diamantina National Park; the Marimbus/Iraquara Environmentally Protected Area; the Serra do Barbado Environmentally Protected Area, in the municipality of Abaíra; Sete Passagens State Park, in the municipality of Miguel Calmon; and the Cachoeira do Ferro Doido Monument), as well as in areas external to conservation units. National herbaria with representative collections of bryophyte of this region were consulted: the Alexandre Leal Costa Herbarium (code, ALCB), affiliated with the Federal University of Bahia Institute of Biology; the Herbarium of the Estate University of Feira de Santana (HUEFS), in the state of Bahia; the Herbarium of the Center for Cacao Research (CEPEC), in the state of Bahia; the Herbarium of the Botanical Institute of São Paulo (SP); and the University of São Paulo Herbarium of Phanerogamae (acronym, SPF). In addition, the species list was supplemented with data from the literature (Yano 1981, 1984, 1989a, 1995, 1996a, 2006, 2008; Yano & Bastos 1994; Harley 1995; Bastos et al. 1998a, 2000; Yano & Peralta 2006; Peralta & Vital 2006; Ballejos & Bastos 2009a, 2009b). Regardless of the source (herbaria or literature), we analyzed only those data related to samples for which there was information about the vegetation formation of origin or elevation. Overall, approximately 2300 samples were analyzed, covering nine cities within the Chapada Diamantina ecoregion: in the north (Morro do Chapéu, Miguel Calmon and Jacobina); in the south (Abaíra, Rio de Contas and Piatã); and in the center (Lençóis, Palmeiras and Mucugê).

Study material and data analysis

The taxa identification was based mainly on Crum (1984), Yano et al. (1985), Frahm (1991), Reese (1993), Zander (1993), Sharp et al. (1994), Buck (1998), Gradstein et al. (2001), Gradstein & Costa (2003) and Pursell (2007). We adopted the classification systems presented by Goffinet et al. (2009) for mosses and by Crandall-Stotler et al. (2009) for liverworts. The taxa authority name abbreviations were based on Brummitt & Powell (1992). The Brazilian state abbreviations are in accordance with the Brazilian Institute of Geography and Statistics guidelines. The geographic distribution of species was based on Yano (1981; 1984; 1989; 1995; 1996; 2006; 2008), Bastos & Yano (2009), Ballejos & Bastos (2009a; 2009b), and Forzza et al. (2012).

We performed a comparative analysis between the different bryophyte flora, based on the presence or absence of species, using the Bray-Curtis method and the software PRIMER 5.1 (Clarke & Warwick 1994). To analyze the geographic distribution of the taxa in Brazil, we defined the following categories of species distribution: restricted, occurring in four of fewer states; moderate, occurring in five to nine states; and broad, occurring in ten or more states (Valente & Pôrto 2006). For the analysis of the elevational distribution of the bryophyte flora from the Chapada Diamantina ecoregion, we used the elevational zones established by Oliveira-Filho et al. (2006) for latitudes < 16ºS, in which lowland formations are defined as occurring at elevations < 400 m; premontane formations are defined as occurring at elevations of 400-800 m; lower montane formations are defined as occurring at elevations of 800-1200 m; and upper montane formations are defined as occurring at elevations > 1200 m. However, we evaluated only the last three of those zones.

Results and discussion

We identified a total of 400 taxa (Tab. 1). Moss species predominated over liverworts in all phytophysiognomies, except in the forest. Species richness and the number of exclusive taxa were greatest in the forests (272 species, 157 exclusive), followed by campos rupestres (212 species, 93 exclusive), caatinga (29 species, 18 exclusive) and Cerrado (20 species, three exclusive). This result was predictable, because the bryophyte composition and richness reflect the environmental conditions in each phytophysiognomy. We should point out that the caatinga and the cerrado, when compared with the forest and the campos rupestres, present conditions that are much more restrictive for the development and establishment of most bryophyte species, mainly due to low humidity and high light intensity. Although the campos rupestres could also be considered restrictive, humidity from the frequent occurrence of fog and from localized accumulations of water, as well as the quite rugged topography, in which there are numerous rock clefts, provides a myriad of microhabitats that are favorable to the growth of the bryophyte flora adapted to those conditions.

As a result of the analysis of bryophyte flora similarity among the phytophysiognomies, we identified clusters in which the forests and campos rupestres shared 46% of the species, compared with only 15% for the cerrado and caatinga. This might be explained by the previously mentioned factors (higher humidity presence and shaded microhabitats) in forests and campos rupestres.

In the forests, Lejeuneaceae, Plagiochilaceae, Radulaceae, Leucobryaceae, Sematophyllaceae and Orthotrichaceae were the most representative families in terms of the number of species. These families are typical of tropical rain forests (Pócs 1982; Richards 1984; Gradstein & Pócs 1989; Gradstein 1995; Gradstein et al. 2001). The majority of their constituents are adapted to the low-light conditions, like most bryophytes, with leaves consisting of a single layer of cells and chlorophyll-containing cells directly exposed to the light. However, such species have a low chlorophyll a/b ratio, are capable of adjusting their number of chloroplasts according to the levels of light and are poikilohydric, having the ability to rehydrate rapidly (Glime 2007).

In campos rupestres, the most representative families were Lepidoziaceae, Pallaviciniaceae, Jungermanniaceae, which also include members with high demand for shaded areas and humidity, as well as Sphagnaceae, Bartramiaceae, Calymperaceae and Leucobryaceae. The latter group includes species with morphological and physiological adaptations to high light intensity and desiccation and therefore have a better chance of enduring prolonged exposure to sunlight, such adaptations including the presence of hyaline cells, which filter the light reaching the photosynthesis cells; cancellinae, for water storage; and hydroids, cells that constitute the water conduction and support tissues (Glime 2007; Proctor 2007).

The particularities of the environmental conditions of the caatinga allow the occurrence of families such as Ricciaceae, which are adapted to the typical arid conditions of the region (Jovet-Ast 1991). Species of the genus Riccia, which are common residents of ephemeral habitats, absorb water by capillarity among the rhizoids on the inferior surface of the thallus. Under drought conditions, the gametophyte furls itself, exposing the rhizoids, which serve to absorb water and provide a reflective surface that protects the chlorophyll-containing cells of the thallus. Some species are capable of surviving for seven years in this desiccated state, and even if the vegetative part dies, the spores can persist because of the great quantity of nutrients they store. The annual species compensate for this water loss by producing a large number of spores and using their ornamentation to attract animals for their dispersion (Glime 2007; Vanderpoorten & Goffinet 2009). As in the present study, other floristic studies of bryophytes in the caatinga (Pôrto et al. 1994; Bastos et al. 1998b) have shown low species richness, with representative species typically being tolerant of exposure to intense light and heat, such as those of the families Pottiaceae and Ricciaceae. A little over one third of the species recorded in the present study were also included in the flora listed in the literature cited above.

We found no families that were exclusive to the cerrado, and the flora of our study sites had low floristic affinity with those described in other studies of the cerrado in northeastern Brazil (Vilas Bôas-Bastos & Bastos 1998; Castro et al. 2002). It is noteworthy that the areas of cerrado investigated in our study were quite dry, and some bore evidence of recent fires.

Among the bryophytes we identified in the Chapada Diamantina ecoregion, the geographic distribution in Brazil was categorized as restricted for 30% of the taxa, moderate for 32% and broad for 38%. Many of the taxa classified as having a restricted or moderate distribution had previously been recorded only for the southeastern region of Brazil, particularly in mountainous areas, where environmental conditions, such as the mild temperatures and cloud cover associated with the upper elevations, enable the survival of species less tolerant to heat and desiccation. This corroborates the findings of Nascimento et al. (2010) regarding the floristic and biogeographical relationships between the arboreal flora of the upper montane forests in the south of the Chapada Diamantina ecoregion and those of the seasonal forest and rain forest formations in the Atlantic Forest of southeastern and southern Brazil, those authors having identified great floristic affinity between the two regions. In that same study, the authors point out a floristic continuation between the Serra do Espinhaço, to the south, and the central-south portion of the Chapada Diamantina ecoregion, as well as the occurrence of an extensive biogeographical province that connects the Chapada Diamantina ecoregion with the Serra da Mantiqueira, forming a corridor composed of campos rupestres and shrub-tree vegetation. That corridor would allow the transit of plant and animal species adapted to grassland and forest environments, where the humidity is higher and the temperatures are milder.

Our analysis of the worldwide geographical distribution of the bryophyte species identified showed a predominance of neotropical species (42%), followed by disjunct species (12%); cosmopolitan species (10%); pantropical species (9%); and species endemic to Brazil (4%), to the American tropics (3%) and to the American subtropics America (8%). In the upper elevations of the Chapada Diamantina ecoregion, there was a significant number of disjunct species with the distribution pattern eastern Brazil-Andes region (14 species), as previously observed for mountainous regions in southeastern Brazil (Santos & Costa 2010b), which can be explained by the similarities in climatic conditions between eastern Brazil and the Andes region. Such species, all of which were sampled in campos rupestres or forests, included Chiloscyphus latifolius (found in Brazil and Bolivia); Radulatenera, Sematophyllumtequendamense,Syrrhopodonhelicophyllus and Syzygiellaliberata (found in Brazil and Colombia); Radulasinuata (found in Brazil, Bolivia and Colombia); Metzgeriahegewaldii (found in Brazil and Peru); Micropterygiumreimersianum (found in Brazil and Venezuela); Micropterygiumcampanense (found in Brazil, Venezuela and Peru); Lepidoziabrasiliensis (found in Brazil, Colombia, Ecuador and Peru); Calypogeia andicola (found in Brazil, Colombia and Ecuador); Lepidozia inaequalis (found in Brazil, Ecuador, Bolivia and Peru); Plagiochila fragilis - (found in Brazil and Ecuador); and Drepanolejeuneacampanulata (found in Brazil and the northern Andes). Other disjunctions were represented by Adelothecium bogotense (found throughout the neotropics, as well as in Madagascar and Tanzania); Aphanolejeunea asperrima (found in Brazil and Patagonia; Archidium clavatum (found in Brazil and Australia); Riccia vitalii (found in Brazil and Costa Rica); Radula cubensis and R. wrightii (found in Brazil and Cuba); Diplasiolejeunea latipuense (found in Brazil and Guyana); Microlejeunea cystifera (found in Brazil and French Guyana); Acroporium caespitosum and Wijkiaflagellifera (found in Brazil and the West Indies); Neesioscyphus homophyllus (found in southeastern Brazil and northern Argentina); Eccremidium floridanum (found in Brazil and the United States); Daltonia pulvinata (found throughout the neotropics and on Reunion Island); Schlotheimia tecta (found throughout the neotropics and in India); Jamesoniella rubricaulis (found throughout the neotropics and in the Azores); and Bryum paradoxum (found throughout the neotropics and in Asia).

Four of the taxa identified are endemic to the Chapada Diamantina ecoregion, all of them belonging to the family Sphagnaceae and sampled in campos rupestres: Sphagnum chi-chiense var. uvidulum; S. harleyi; S. contortulum; and S. vitalii.

Bryophyte composition differed among the three elevational zones studied, species richness and the numbers of exclusive taxa being highest in the lower and upper montane formations: premontane (40 species, seven exclusive); lower montane (246 species, 121 exclusive), upper montane (241 species, 96 exclusive). Only eight taxa were sampled in all three zones; the premontane and lower montane zones had 33 taxa in common; and the lower and upper montane zones had 51 taxa in common.

The bryophyte flora found in the upper montane elevational zone of the Chapada Diamantina ecoregion comprise taxa previously identified as typical of mountainous regions in Brazil (Gradstein & Costa 2003; Costa & Lima 2005; Santos & Costa 2010a): Adelanthus decipiens, Aptychopsis pyrrophylla, Atractylocarpus brasiliensis,Campylopus dichrostis,C. julicaulis, Drepanolejeunea araucariae, Frulania arecae,Herbertus juniperoideus ssp. bivittatus,Harpalejeunea subacuta, Jamesoniella rubricaulis, Jungermannia sphaerocarpa, Microlejeunea cystifera, Neesioscyphus homophyllus, Odontoschisma denudatum,Plagiochila cristata, Polytrichum brasiliense,Rhacocarpus purpurascens,Radula fendleri, Saccogynidium caldense,Schloteimia trichomitria,Sphagnum alegrense,Syzygiella aff. integerrima, S. liberata and Trichocolea flaccida.

Among the species that occurred in the lower and upper montane formations and those of restricted distribution in Brazil, some are distinctive for their rarity within the Chapada Diamantina ecoregion, having been collected in forests or campos rupestres areas, with only one to five occurrences: Adelothecium bogotense,Anastrophyllum piligerum, Harpalejeuneasubacuta,Jungermanniasphaerocarpa, Lophocolea mandonii, Micropterygium campanense, Neesioscyphushomophyllus, Odontoschisma brasiliense,Sematophyllumswartzii,Sphagnum alegrense and Syzygiella liberata. Some of those species have been listed as threatened in other Brazilian states.

Based on the results of this study, we conclude that the Chapada Diamantina ecoregion is an important center of bryophyte diversity, with high species richness, representing approximately 63% of the bryophyte flora of Bahia. A considerable proportion (83%) of the species identified were exclusive to montane zones (lower and upper), 30% being exclusive to the upper montane zone, mainly distributed in montane forests and campos rupestres. Despite its geological, ecological and biological importance, as well as its considerable size, to date only nine conservation units have been established in the region, representing only 8.1% of its area, and only three of those are totally protected areas, corresponding to a mere 3.9% of its total area (MMA 2005). Therefore, we can highlight the importance of preserving this region and of reducing the destructive impact of human activity, not only in the three areas already recognized for their high levels of diversity (the Serra do Barbado Environmentally Protected Area; Sete Passagens State Park; and Chapada Diamantina National Park) but also in the campos rupestres, seasonal forests and rain forests of the surrounding areas such as the municipalities of Piatã and Morro do Chapéu.

Acknowledgments

This study received financial support from the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development; Doctoral Scholarship Grant to E.B.V.) and from the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB, Foundation for the Support of Research in the State of Bahia; Grant no. APR 0066/2007). The authors are grateful to the Federal University of Feira de Santana Department of Biological Sciences for providing access to the infrastructure necessary for the execution of the study (Mycology Laboratory and Herbarium).

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Submitted: 20 August, 2012

Accepted: 17 December, 2012

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  • *
    Author for correspondence:
  • 1
    Based on the Doctoral thesis of the first Author
  • Publication Dates

    • Publication in this collection
      22 July 2013
    • Date of issue
      June 2013

    History

    • Received
      20 Aug 2012
    • Accepted
      17 Dec 2012
    Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
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