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Host-exclusivity and host-recurrence by wood decay fungi (Basidiomycota - Agaricomycetes) in Brazilian mangroves

ABSTRACT

This study aimed to investigate for the first time the ecological interactions between species of Agaricomycetes and their host plants in Brazilian mangroves. Thirty-two field trips were undertaken to four mangroves in the state of Pernambuco, Brazil, from April 2009 to March 2010. One 250 x 40 m stand was delimited in each mangrove and six categories of substrates were artificially established: living Avicennia schaueriana (LA), dead A. schaueriana (DA), living Rhizophora mangle (LR), dead R. mangle (DR), living Laguncularia racemosa (LL) and dead L. racemosa (DL). Thirty-three species of Agaricomycetes were collected, 13 of which had more than five reports and so were used in statistical analyses. Twelve species showed significant values for fungal-plant interaction: one of them was host-exclusive in DR, while five were host-recurrent on A. schauerianna; six occurred more in dead substrates, regardless the host species. Overall, the results were as expected for environments with low plant species richness, and where specificity, exclusivity and/or recurrence are more easily seen. However, to properly evaluate these relationships, mangrove ecosystems cannot be considered homogeneous since they can possess different plant communities, and thus different types of fungal-plant interactions.

Keywords
Fungi; estuaries; host-fungi interaction; host-relationships; plant-fungi interaction

Introduction

Wood decay fungi are mostly macroscopic Basidiomycota usually known as mushrooms, bracket fungi and earthstars. They occur in different habitats, being found with higher frequency and abundance in forests. They are able to degrade lignin and/or cellulose, having an essential role to the nutrient cycle of the environment. Some of them establish close relationship with the substrate and can be considered host-specific to the plant that they decay (Kendrick 2000Kendrick B. 2000. The fifth kingdom. 2nd. edn. Newburyport, MA: Focus Information Group. ; Deacon 2006Deacon JW. 2006. Fungal biology. 4th. edn. Malden, Blackwell Publishing. ; Webster & Weber 2007Webster J, Weber RWS. 2007. Introduction to Fungi. 3rd. edn. Cambridge, Cambridge University Press.).

About the terms used for the ecological relationships between saprobe fungi and living or dead hosts, Zhou & Hyde (2001Zhou D, Hyde KD. 2001. Host-specificity, host-exclusivity, and host-recurrence insaprobic fungi. Mycological Ressearch 5: 1449-1457.) proposed a redefinition of these terms. The term “specificity” would imply in the relationship between a living host and a fungus, thus, would not be applied to the saprophytic species; the term “exclusivity” would be the exclusive occurrence of a saprobe in a particular host groups, while “recurrence” would be the frequent or predominant occurrence of a parasitic or saprobe fungus in a particular host or host groups in the same habitat. This last term was previously referred to "preference" (Lindblad 2000Lindblad I. 2000. Host specificity of some wood-inhabiting fungi in a tropical forest. Mycologia 92: 399-405. ; Gilbert and Sousa 2002Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404. ; Gilbert et al. 2008Gilbert GS, Gorospe J, Ryvarden L. 2008. Host and habitat preferences of polypore fungi in Micronesian tropical flooded forests. Mycological Research 112: 674-680. ). However, Zhou & Hyde (2001Zhou D, Hyde KD. 2001. Host-specificity, host-exclusivity, and host-recurrence insaprobic fungi. Mycological Ressearch 5: 1449-1457.) suggested that "preference" should not be used for fungi, because it would imply in “act of volition on the part of the fungus”.

The fungal community from a particular environment is related, among other factors, to the substrate availability (plant species composition, for example). So, in low diversity environments, like mangroves, the relationships between fungi and plants would be more easily observed (Gilbert and Sousa 2002Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404. ).

In Brazil, some studies about lignolytic Agaricomycetes in mangroves were published (Sotão et al. 1991Sotão HMP, Bononi VLR, Figueiredo TS. 1991. Basidiomycetes de manguezais da Ilha de Maracá, Amapá, Brasil. Serie Botanica 7: 109-114. ; Almeida Filho et al. 1993Almeida-Filho OM, Bueno R, Bononi VLR. 1993. Algumas espécies de fungos basidiomicetos dos manguezais do Estado de São Paulo. Hoehnea 20: 87-92. ; Gugliotta & Capelari 1995Gugliotta AM, Capelari M. 1995. Polyporaceae from Ilha do Cardoso, SP, Brazil. Mycotaxon 56: 107-113. ; Campos and Cavalcanti 2000Campos EL, Cavalcanti MAQ. 2000. Primeira ocorrência de Phellinus mangrovicus (Imaz.) Imaz. para o Brasil. Acta Botanica Brasilica 14: 263-265.; Campos et al. 2003Campos EL, Sotão HMP, Cavalcanti MAQ, Luz AB. 2003. Basidiomycetes de manguezais da APA de Algodoal-Maiandeua, Pará, Brasil. Boletim do Museu Paraense Emílio Goeldi Série Ciências Naturais 1: 97-102. ; Baltazar et al. 2009Baltazar JM, Trierveiler-Pereira L, Loguercio-Leite CA. 2009. Checklist of xylophilous basidiomycetes (Basidiomycota) in mangroves. Mycotaxon 107: 221-224.; Nogueira-Melo et al. 2014Nogueira-Melo GS, Santos PJP, Gibertoni TB. 2014. The community structure of macroscopic basidiomycetes (Fungi) in Brazilian mangroves influenced by temporal and spatial variations. Revista de Biología Tropical 62:1587-1595. ). However, none of them provided information about the interactions between fungi and mangrove plants.

Thus, this study aimed to investigate and report for the first time the ecological interactions between lignolytic Agaricomycetes and host plants in Brazilian mangroves and to verify if these interactions are significantly different from other mangroves.

Materials and methods

Study site

Brazilian mangroves extend from the state of Amapá (4°30'N) to Santa Catarina (28°30'S), varying significantly in plant growth form, species distribution patterns, and stand structure, in spite of the limited floristic diversity (Schaeffer-Novelli, 1995Schaeffer-Novelli, Y. 1995. Manguezal ecossistema entre a terra e o mar. São Paulo, Caribbean Ecological Research.). Five species of mangrove trees are recorded in the Northeast region: Rhizophora mangle L., Avicennia schaueriana Stapf. and Leech, A. germinans L., Laguncularia racemosa (L.) Gaertn and Conocarpus erectus L. (Cintrón & Schaeffer-Novelli 1992Cintrón G, Schaeffer-Novelli Y. 1992. Ecology and management of new world mangroves. In: Seeliger U. (ed.) Coastal plant communities of Latin America. New York, Academic Press. p. 233-258. ).

The study was conducted in four mangroves in the state of Pernambuco, Northeast Brazil: Ariquindá river (AR) (35°06'6"W and 08°41'28"S), Mangrove at Maracaípe river (MA) (35°00'29"W and 08°32'22.8"S), Mangrove at Santa Cruz Chanel (SC) (07°46'52.61"S and 34°52'53.3"W) and Mangrove at Timbó river (TI) (07°51'24.8"S and 34°50'32.7"W). The studied areas are fringe-type mangrove forests, as they develop along the margins of protected coasts (Cintrón & Schaefer-Novelli 1980Cintrón G, Schaeffer-Novelli Y. 1980. Introducción a la ecologia del manglar. São Paulo, Instituto Oceanográfico USP.), and are basically composed of R. mangle, A. schaueriana and L. racemosa (Schuler et al. 2000Schuler CAB, Andrade VC, Santos DS. 2000. O manguezal: composição e estrutura. In: Barros HM, Esquinazi L, Macedo SJ, Lima T. (eds.) Gerenciamento participativo de estuários e manguezais. Recife, Editora Universitária da Universidade Federal de Pernambuco. p. 89-102. ). In this study, the mangroves SC and TI had predominance of A. schaueriana, while AR and MA of R. mangle.

The climate in these areas is defined by Köepen-Geiger classification as a borderline between tropical monsoon (Am) and tropical wet and dry savanna (As instead of Aw, when the dry season occurs during the time of higher sun and longer days) (Peel et al. 2007Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633-1644. ; Chen & Chen 2013Chen AD, Chen HW. 2013. Using the Köppen classification to quantify climate variation and change: An example for 1901-2010. Environmental Development. 6: 69-79. ).

Basidiomata collections and field sampling procedure

For basidiomata collection, one stand of 10 000 m² (40 × 250 m) was established in each mangrove using the Global Positioning System - GPS. Eight surveys in each stand were undertaken (April to September 2009, December 2009 and March 2010, totaling 32 surveys) and all basidiomata were collected.

For the estimate of the proportion of available living and dead substrate, an imaginary line of 250 m was delimited inside each stand. On the starting (0 m), intermediate (125 m) and final points (250 m), three other lines of 40 m long (20 m on each side) were delimitated perpendicularly to the main line. The living or dead substrate present in these lines, with or without basidiomata, were quantified. The values for each line were summed and the proportion of each species and condition of the substrate were calculated for each stand. Based on the plant species in the studied areas, six categories of substrate were proposed: living A. schaueriana (LA), dead A. schaueriana (DA), living R. mangle (LR), dead R. mangle (DR), living L. racemosa (LV) and dead L. racemosa (LM). Fungi found on dead parts of living plants were considered as degrading dead tissue.

Taxonomy

After collections, the specimens were analyzed macro- (shape, color, hymenial surface) and micromorphologically (hyphal system, presence/absence and measurements of sterile structures and basidiospores). Microscopical observations were made from slide preparations with 5 % KOH, stained with 1 % of aqueous phloxine, and Melzer’s reagent (Ryvarden 1991Ryvarden L. 1991. Genera of polypores, nomenclature and taxonomy. Synopsis Fungorum 5. Oslo, Fungiflora.). Color designation followed Watling (1969Watling R. 1969. Colour Identification Chart. Edinburgo, Her Majesty’s Stationary Office. ). The material was identified using specialized literature (Ryvarden & Johansen 1980Ryvarden L, Johansen I. 1980. A preliminary polypore flora of East Africa. Oslo, Fungiflora. ; Gilbertson & Ryvarden 1986Gilbertson RL, Ryvarden L. 1986. North American Polypores Vol. 1. Oslo, Fungiflora. ; Hjortstam et al. 1987Hjortstam K, Larsson KH, Ryvarden L. 1987. The Corticiaceae of North Europe Vol. 1. Oslo, Fungiflora. ; 1988Hjortstam K, Larsson KH, L Ryvarden. 1988. The Corticiaceae of North Europe Vol. 2. Oslo, Fungiflora.; Hjortstam & Ryvarden 1990Hjortstam K, Ryvarden L. 1990. Lopharia and Porostereum (Corticiaceae) Synopsis Fungorum 4. Oslo, Fungiflora. ; Boidin et al. 1997Boidin J, Lanquetin P, Gilles G. 1997. Le genre Gleocystidiellum sensu latu (Basidiomycotina). Bulletin de la Societé Mycologique de France 113.; Boidin & Gilles 2000Boidin J, Gilles G. 2000. Basidiomycetes Aphyllophorales de L’ile de la reunion XXI - Suíte. Mycotaxon 75: 357-387. ; Ryvarden 2004Ryvarden L. 2004. Neotropical Polypores. Part 1. Synopsis Fungorum 19. Oslo, Fungiflora.) and incorporated to the Herbarium URM. The nomenclature for Agaricomycetes followed the Index Fungorum (www.indexfungorum.org).

Statistical Analyses

Species abundance values were represented by the number of occurrence of specimens/individuals on each substrate; one specimen/individual may be represented by several basidiomata (Nogueira-Melo et al. 2014Nogueira-Melo GS, Santos PJP, Gibertoni TB. 2014. The community structure of macroscopic basidiomycetes (Fungi) in Brazilian mangroves influenced by temporal and spatial variations. Revista de Biología Tropical 62:1587-1595. ). For the analysis, we considered the species with more than five specimens to reduce error type II probability. The binomial probability test was applied to the species occurrences using BioEstat 5.0 program (Ayres et al. 2007Ayres M, Ayres JRM, Ayres DL, Santos AAS. 2007. BioEstat: Aplicações estatísticas nas áreas de ciências biomédicas. 5th. edn. Belém, Guanabara.). The level of significance was set at p < 0.05 for all analyses.

Results and discussion

Three hundred seventy two plants were counted, 135 belonging to LR, 111 to DR, 86 to LA, 35 to DA, four to LL and one to DL. It was observed that the mangrove areas differ in the proportion of plant substrate, with predominance of LR in Rio Formoso (74), DR in Maracaípe (63) and LA in Maria Farinha and Itamaracá (48 and 38 respectively). Two hundred seventy four specimens belonging to 33 species of Agaricomycetes were collected (Tab. 1, Fig. 1). The occurrence values of Agaricomycetes in L. racemosa were not considered in the analysis, since the low number of individuals of this plant species may cause distortion or overestimation of p values.

Table 1
Lignolytic Agaricomycetes abundance by substrate category in Pernambuco mangroves. DR = dead Rhizophora mangle; DA = dead Avicennia schaueriana; LA = living A. schaueriana; LR = living R. mangle; LL = living Laguncularia racemosa; DL = dead L. racemosa.

Figure 1
Number of individuals of mangrove plants and fungi by substrate category. DR = dead Rhizophora mangle; DR = dead Rhizophora mangle; DA = dead Avicennia schaueriana; LA = living A. schaueriana; LR = living R. mangle; LL = living Laguncularia racemosa; DL = dead L. racemosa.

Thirteen species occurred more than five times and were sufficiently abundant for the analysis (Tab. 2). Except for C. molle, whose occurrence values did not differ between the substrate categories, 12 species presented significant p-values. Coriolopsis hostmanii, H. amethystea, S. commune e T. biforme occurred mainly in DA, while G. striatum, in DR. Besides, F. nivosa, H. hydnoides, H. iguazuense, P. gilvus, P. guyanensis, S. paradoxa and T. detrita occurred more than expected in dead substrates, regardless of the plant species (Tab. 2).

Table 2
Lignolytic Agaricomycetes considered for the analysis of predominance by substrate category. Lignolytic Agaricomycetes considered for the analysis of predominance by substrate category. DR = dead Rhizophora mangle; DA = dead Avicennia schaueriana; LA = living A. schaueriana; LR = living R. mangle; pHS = level of significance for host species; pCS = level of significance for condition of the substrate (dead or living); pHS = level of significance for host species; pCS = level of significance for condition of the substrate (dead or living).

Except for C. molle, all the abundant species for ecological analysis occurred significantly more in dead substrates (Tab. 2). This is expected for lignolytic Agaricomycetes which are, in general, saprophytic and degrade dead plant tissue being the main agents decomposing trees of the forest (Kendrick 2000Kendrick B. 2000. The fifth kingdom. 2nd. edn. Newburyport, MA: Focus Information Group. ; Webster and Weber 2007Webster J, Weber RWS. 2007. Introduction to Fungi. 3rd. edn. Cambridge, Cambridge University Press.).

Additionally, the wood characteristics may also influence the occurrence of wood decay fungi found in this study. For example, even with the higher frequency of LR on the studied transects, which could have influenced the host-specificity, the test showed that no species occurred in living substrates. This observation was more evident in R. mangle than A. schauerianna. Rhizophora species are known as great producers of tannin, a compound not produced by Avicennia species (Erickson et al. 2004Erickson AA, Bell SS, Dawes CJ. 2004. Does mangrove leaf chemistry help explain crab herbivory patterns?. Biotropica 36: 333-343. ). Rhizophora mangle has 20 to 30% of the compound in the bark, which characterizes the reddish color of the trunk (Haslam 1966Haslam E. 1966. Chemistry of vegetable tanins. London, Academy Perss. ). The tannin is a phenolic compound produced by the plant, considered a potent inhibitor of enzymes, of processes of decay and of attack by herbivores and phytopathogenic microorganisms. When the plant dies, the tannin levels fall, enabling the growth of decomposer fungi and other organisms (Silva & Silva 1999Silva MR, Silva MAAP. 1999. Aspectos nutricionais de fitatos e taninos. Revista de Nutrição 12: 5-19. ).

Based on the concepts proposed by Zhou & Hyde (2001Zhou D, Hyde KD. 2001. Host-specificity, host-exclusivity, and host-recurrence insaprobic fungi. Mycological Ressearch 5: 1449-1457.), in our study, host-exclusivity and host-recurrence were found. No host-specificity was observed. Six of the 13 analyzed species showed predominance in one of the host categories. Gloeophyllum striatum was host-exclusive in R. mangle, while C. hostmanii, H. amethystea, P. gilvus, S. commune and T. biforme were host-recurrence in A. schauerianna.

Similar results were also obtained by Gilbert & Sousa (2002Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404. ) and Gilbert et al. (2008Gilbert GS, Gorospe J, Ryvarden L. 2008. Host and habitat preferences of polypore fungi in Micronesian tropical flooded forests. Mycological Research 112: 674-680. ). In mangroves of Panama, Gilbert & Sousa (2002Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404. ) found nine sufficiently abundant Agaricomycetes for statistical analysis, of which five showed host-preference (host-recurrence sensuZhou & Hyde 2001Zhou D, Hyde KD. 2001. Host-specificity, host-exclusivity, and host-recurrence insaprobic fungi. Mycological Ressearch 5: 1449-1457.) in three plant species, while in mangroves of Micronesia, Gilbert et al. (2008Gilbert GS, Gorospe J, Ryvarden L. 2008. Host and habitat preferences of polypore fungi in Micronesian tropical flooded forests. Mycological Research 112: 674-680. ) reported host-recurrence between five species of Agaricomycetes and three plant species.

In Brazil, host-specificity has already been reported by Drechsler-Santos et al. (2010Drechsler-Santos ER, Santos PJP, Gibertoni TB, Cavalcanti MAQ. 2010. Ecological aspects of Hymenochaetaceae in an area of Caatinga (semi-arid) in Northeast Brazil. Fungal Diversity 42: 71-78. ) in the Caatinga [a Brazilian ecoregion characterized mostly by the xerophytic vegetation and hot and dry (BSh) climate], where Phellinotus piptadeniae was differentially frequent on Piptadenia moniliformes and Phellinotus neoaridus on Caesalpinia microphylla.

Of the collected species, only P. mangrovicus seems to be restricted to mangroves (Larsen & Cobb-Poulle 1990Larsen M, Cobb-Poule LA. 1990. Phellinus (Hymenochaetaceae). A survey of the world taxa Synopsis Fungorum 3. Oslo, Fungiflora. ; Campos and Cavalcanti 2000Campos EL, Cavalcanti MAQ. 2000. Primeira ocorrência de Phellinus mangrovicus (Imaz.) Imaz. para o Brasil. Acta Botanica Brasilica 14: 263-265.; Ryvarden 2004Ryvarden L. 2004. Neotropical Polypores. Part 1. Synopsis Fungorum 19. Oslo, Fungiflora.), but it was not sufficiently abundant for statistical analysis. The other species are considered host-generalists, (including G. striatum, which in the current study was host-exclusive in R. mangle), being mentioned previously in other hosts when collected in high-diverse ecosystems (Ryvarden & Johansen 1980Ryvarden L, Johansen I. 1980. A preliminary polypore flora of East Africa. Oslo, Fungiflora. ; Hjortstam et al. 1987Hjortstam K, Larsson KH, Ryvarden L. 1987. The Corticiaceae of North Europe Vol. 1. Oslo, Fungiflora. ; Gilbertson & Ryvarden 1986Gilbertson RL, Ryvarden L. 1986. North American Polypores Vol. 1. Oslo, Fungiflora. ; Hjortstam & Ryvarden 1990Hjortstam K, Ryvarden L. 1990. Lopharia and Porostereum (Corticiaceae) Synopsis Fungorum 4. Oslo, Fungiflora. ; Boidin et al. 1997Boidin J, Lanquetin P, Gilles G. 1997. Le genre Gleocystidiellum sensu latu (Basidiomycotina). Bulletin de la Societé Mycologique de France 113.; Boidin & Giles 2000Boidin J, Gilles G. 2000. Basidiomycetes Aphyllophorales de L’ile de la reunion XXI - Suíte. Mycotaxon 75: 357-387. ; Lindblad 2000Lindblad I. 2000. Host specificity of some wood-inhabiting fungi in a tropical forest. Mycologia 92: 399-405. ).

The data here presented may support the hypothesis of Gilbert & Sousa (2002Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404. ) that in environments of low diversity, such as mangroves, the differential occurrence of a fungus in a host may happen more easily, since in those environments plant diversity is low and, therefore, the number of suitable host plants is higher.

Overall, the results were those expected for environments with low richness of plants, since about half of the species sufficiently abundant for the statistical analyses occupied differentially one of the established categories of substrate. However, to evaluate these relationships, the mangrove cannot be considered as a homogeneous ecosystem because there are many factors that influence locally the distribution and composition of plant species, which, in turn, will influence the distribution of fungi.

Acknowledgements

The authors would like to thank the laboratory colleagues during the field trips; Leif Ryvarden and Karl-Henrik Larsson for identifying some species; and Miles Hudson for English improvements. This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, master scholarship of GSNM) and by FACEPE (APQ 0444-2.03/08).

References

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  • Ayres M, Ayres JRM, Ayres DL, Santos AAS. 2007. BioEstat: Aplicações estatísticas nas áreas de ciências biomédicas. 5th. edn. Belém, Guanabara.
  • Baltazar JM, Trierveiler-Pereira L, Loguercio-Leite CA. 2009. Checklist of xylophilous basidiomycetes (Basidiomycota) in mangroves. Mycotaxon 107: 221-224.
  • Boidin J, Gilles G. 2000. Basidiomycetes Aphyllophorales de L’ile de la reunion XXI - Suíte. Mycotaxon 75: 357-387.
  • Boidin J, Lanquetin P, Gilles G. 1997. Le genre Gleocystidiellum sensu latu (Basidiomycotina). Bulletin de la Societé Mycologique de France 113.
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  • Chen AD, Chen HW. 2013. Using the Köppen classification to quantify climate variation and change: An example for 1901-2010. Environmental Development. 6: 69-79.
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  • Erickson AA, Bell SS, Dawes CJ. 2004. Does mangrove leaf chemistry help explain crab herbivory patterns?. Biotropica 36: 333-343.
  • Gilbert GS, Gorospe J, Ryvarden L. 2008. Host and habitat preferences of polypore fungi in Micronesian tropical flooded forests. Mycological Research 112: 674-680.
  • Gilbert GS, Sousa WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404.
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  • Gugliotta AM, Capelari M. 1995. Polyporaceae from Ilha do Cardoso, SP, Brazil. Mycotaxon 56: 107-113.
  • Haslam E. 1966. Chemistry of vegetable tanins. London, Academy Perss.
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  • Nogueira-Melo GS, Santos PJP, Gibertoni TB. 2014. The community structure of macroscopic basidiomycetes (Fungi) in Brazilian mangroves influenced by temporal and spatial variations. Revista de Biología Tropical 62:1587-1595.
  • Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633-1644.
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Publication Dates

  • Publication in this collection
    21 Sept 2017
  • Date of issue
    Oct-Dec 2017

History

  • Received
    07 Apr 2017
  • Accepted
    09 May 2017
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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