The community structure of macroscopic basidiomycetes (Fungi) in Brazilian mangroves influenced by temporal and spatial variations
La estructura de la comunidad de basidiomicetos macroscópicos (Fungi) en los manglares brasileños influenciada por las variaciones temporales y espaciales
Georgea Santos Nogueira-Melo1*, Paulo Jorge Parreira Santos2* & Tatiana Baptista Gibertoni1
Abstract
Mangroves are transitional ecosystems between terrestrial and marine environments, and are distinguished by a high abundance of animals, plants, and fungi. Although macrofungi occur in different types of habitat, including mangroves, little is known about their community structure and dynamic. Therefore the aim of this study was to analyze the diversity of macrofungi in a number of Brazilian mangroves, and the relationship between such diversity, precipitation and area of collection. A total of 32 field trips were undertaken from 2009 to 2010, and macrofungi were studied in four 250×40m transects: Timbó and Santa Cruz Channel on the Northern coast, and Maracaípe and Ariquindá on the Southern coast. All basidiomata found along the transects were placed in paper bags, air-dried and identified using existing literature. It was found that Northern areas predominantly featured Avicennia schaueriana mangroves, while Rhizophora mangle dominated in Southern transects. A total of 275 specimens were collected, and 33 species, 28 genera, 14 families and six orders were represented. Overall abundance and species richness did not vary significantly among areas, but varied according to time, being higher during the rainy season. Subtle differences in composition were observed over time and between areas, probably due to variations in plant species occurrence. Further studies with collections during months of greater precipitation in transects dominated by different mangrove species of the same ecosystem are suggested to assess the overall diversity of mycobiota in these ecosystems.
Los manglares son ecosistemas de transición entre los ambientes terrestres y marinos, y se distinguen por la gran abundancia de animales, plantas y hongos. Aunque los macrohongos se encuentran en diferentes tipos de hábitat, incluidos los manglares, poco se sabe acerca de la estructura de su comunidad y dinámica. Por lo tanto, el objetivo de este estudio fue analizar la diversidad de macrohongos en los manglares de Brasil y su relación con la precipitación y área de recolección. Se realizaron un total de 32 salidas de campo entre 2009 y 2010, y los macrohongos fueron estudiados en cuatro transectos de 250×40m: Timbó y Canal de Santa Cruz en la costa norte y Maracaípe y Ariquindá en la costa sur. Todos los basidiomas encontrados a lo largo de los transectos se colocaron deshidratados en bolsas de papel, y se identificaron con ayuda de la literatura preexistente. Se encontró que las zonas del norte predominantemente presentaron Avicennia schaueriana, mientras Rhizophora mangle domina en transectos del sur. Se recolectaron un total de 275 especímenes y 33 especies, 28 géneros, 14 familias y seis órdenes estuvieron representados. Abundancia y riqueza de especies en general no varió significativamente entre las áreas, pero si varió en el tiempo, siendo mayor durante la estación lluviosa. Se observaron diferencias sutiles en la composición a través del tiempo y entre áreas, probablemente debido a las variaciones en la presencia de las especies de plantas. Otros estudios con recolectas durante los meses de mayor precipitación en transectos dominados por diferentes plan- tas de manglar en el mismo ecosistema son deseables para acceder a la diversidad de la micobiota.
Macrofungi occur in different habitat types, including mangroves, and are found with higher frequency and diversity in tropical ]]>
]]>
Despite the importance of decaying wood fungi, little is known about their community structure and dynamic in mangroves. Information of the distribution patterns and the factors that control or limit their diversity in such environments in tropical areas is scarce (Lindblad, 2000; Lindblad, 2001; Gilbert & Sousa, 2002; Urcelay & Robledo, 2004; Robledo, Urcelay, Domínguez ]]>
The aim of the present study was to determine the structure and describe the specific composition of a ]]>
]]>
Materials and Methods
The study was conducted in four mangrove areas, belonging to four estuaries in the state of Pernambuco in the Northeast of Brazil. Two were ]]>
Avicennia schaueriana predominates; and two along the Southern ]]>
Rhizophora mangle predominates. Northern coast mangroves were surrounded by urban areas, while those from the Southern coast were distant from such areas (Montes, Macêdo & Koening, 2002; Mendonça & Almeida-Cortez, 2007). The Northern mangroves are approximately 45km apart, while those ]]>
Three typical mangrove tree species were frequently found in the study areas: Avicennia schaueriana Stapf. ]]>
Laguncularia racemosa (L.) Gaertn (white mangrove), and Rhizophora mangle L. (red mangrove). In the studied forests, these species are differentially distributed according to distance from the water’s edge, but their distributions overlap to varying degrees (Cintrón & Schaeffer-Novelli, 1980; Schaeffer-Novelli, Cintrón-Molero, Andaime & Camargo, 1990). ]]>
The climate in these areas is defined as tropical humid (Am by Köepen classification), with high monthly and low annual temperature amplitude, an average annual temperature of 21°C and annual precipitation greater than 1 500mm (Peel, Finlayson & McMahon, 2007).
]]>
In order to study fungi in these areas, one transect of 250×40m (10 000m2; 20m to the right and 20m to the left of the transect), starting in the estuary and roughly following a line parallel to the water channel, was established in each mangrove, using Global Position System (GPS). A collection trip was undertaken monthly in each of the four areas for ]]>
All basidiomata found along transects were placed in paper bags and collection data (position, date and substrate) was ]]>
Species ]]>
m2). One specimen/individual may be represented by several basidiomata.
]]>
Statistical analysis was performed in accordance with the methods proposed by Clarke & Warwick (1994) using the PRIMER® 6 (Plymouth Routines in Multivariate Ecological Research) software.
Two-way variance ]]>
]]>
The Bray–Curtis index was applied to standardized data to assess the similarity between replicates. Multi-dimensional scaling (MDS) was used to represent the similarity matrix.
The BioEstat 5.0 method of binomial ]]>
The normal approximation to the binomial test was used to verify the differences among plant proportions in areas using BioEstat 5.0 software. Since six paired comparisons were made, the significance level was set at p<0.01 ]]>
Abiotic factors considered in this study were temperature and rainfall, data of which was provided by the Instituto de Tecnologia de Pernambuco - ]]>
Results
A total of 275 specimens were analyzed, representing 33 species, 28 genera, 14 families and six orders. Of the 14 families, four presented more than 15 records and together constituted 70% of specimens collected: Gloeophyllaceae, with 55 records, was represented only by Gloeophyllum ]]>
; Hymenochaetaceae, which had 25 occurrences of two genera and four species; Polyporaceae, which had 95 occurrences corresponding to nine species and eight genera; and Schizoporaceae, which had 26 records and was represented exclusively by Schizopora paradoxa (Table 1).
From the 275 ]]>
(3;21)=3.324, p=0.015; F(3;21)=1.060, p=0.388, respectively]. ANOSIM revealed subtle differences in the proportion of species of the fungal community among the four mangrove areas (Rglobal=0.384, number of permutations=999, p=0.001), and between the northern (S and T) and southern mangroves (A and M) (Rglobal=0.33, number of permutations=999, ]]>
Fig. 1).
Of the 33 species, four were common to all four areas: G. striatum, P. gilvus, S. paradoxa and T. biforme. ]]>
Table 2, in bold). Coriolopsis hostmanii, P. gilvus and T. biforme were ]]>
H. hydnoides and H. iguazuense in T; P. guyanensis and G. striatum in M, and S. paradoxa in A, while the values of H. amethystea and P. ]]>
were not different from random occurrence levels (Table 2).
The studied areas differed in proportions of mangrove species. Northern coastal transects showed predominance of ]]>
A. schaueriana, while Southern coastal transects presented mostly R. mangle (M×A:Z=1.043, p=0.297; M×S:Z=7.677, p<0.0001; M×T:Z=9.065, p<0.0001; A×S:Z=6.680 p<0.0001; A×T:Z=8.072, p<0.0001; S×T: Z=2.220, p=0.0264).
Average ]]>
Fig. 2).
Of the 275 collected specimens, 30 (=15 species) were found in April, 41 (=17) in May, 53 (=20) in June, 40 (=14) in July, 31 (=16) in August, 35 (=16) in September, 32 (=11) in December and 13 (=six) in March. There was a significant difference in sample richness according to time between June and March ]]>
(3;21)=3.324, p=0.015]. Additionally, there were temporal differences in abundance among the collection periods: May, June, July and September yielded more specimens than March [(F(3;21)=4.055, p=0.006)]. A slight difference in species composition was also observed ]]>
global=0.141, number of permutations=999, p=0.044) when occurrence of fungi in the dry and rainy season were compared.
Discussion
]]>
The present study showed that the relative proportion of macroscopic basidiomycete species was different among the four studied areas, and between the Northern and Southern mangroves. Although the ANOSIM Rglobal value found a statistical significant distinction among areas (Rglobal=0.384 and ]]>
Therefore, the collected species belong to the same community (macrofungi inhabiting mangroves). However, the differential occurrence of about one-third of the 33 collected fungal species in the areas may have contributed to the ]]>
Furthermore, in transects of the Northern mangroves, A. schaueriana was predominant, while R. mangle ]]>
In the present study, the abundance and richness of wood-decaying basidiomycetes (and to a lesser degree composition) were affected by precipitation: more specimens were collected in the rainy season and fewer during the dry season. The influence of precipitation on the occurrence of these macrofungi has ]]>
However, ]]>
Recently, ]]>
The results of the present study ]]>
Acknowledgments
The authors would like to thank their laboratory colleagues for support during the field trips; Leif Ryvarden and Karl-Henrik Larsson for species identification, Robert Lücking and Michael Finnie for English improvement and valuable suggestions, Roger Melo and Lucas Cavalcanti for help with figures. This research was supported by the Conselho Nacional de Desenvolvimento ]]>
References
Alexopoulos, C. J., Mims, C. W., & Blackwell, M. (1996). Introductory Mycology (4th ed.). New York: John Wiley and Sons Press. [ Links ]
Almeida-Filho, O. M., Bueno, R., & Bononi, V. L. R. (1993). Algumas espécies de fungos basidiomicetos dos manguezais do Estado de São Paulo. Hoehnea, 20(1/2), 87-92. [ Links ]
Ayres, M., Ayres, J. R. M., Ayres, D. L., & Santos, A. A. S. (2007). BioEstat: Aplicações estatísticas nas áreas de ciências biomédicas (5th ed.). Belém: Guanabara. [ Links ]
Baltazar, J. M., Trierveiler-Pereira, L., & Loguercio-Leite, C. (2009). A. checklist of xylophilous basidiomycetes (Basidiomycota) in mangroves. Mycotaxon, 107, 221-224. [ Links ]
Boddy, L. & Rayner, A. D. M. (1983). Origins of decay in living deciduous trees: the role of moisture content and a re-appraisal of the expanded concept of tree decay. New Phytology, 94, 623-641. [ Links ]
Boidin, J., Lanquetin, P., & Gilles, G. (1997). Le genre Gleocystidiellum sensu latu (Basidiomycotina). Bulletin trimestriel de la Société mycologique de France, 113. [ Links ]
Boidin, J. & Gilles, G. (2000). Basidiomycètes Aphyllophorales de l’île de la Réunion XXI-suite. Mycotaxon, 75, 357-387. [ Links ]
Campos, E. L. & Cavalcanti, M. A. Q. (2000). Primeira ocorrência de Phellinus mangrovicus (Imaz.) Imaz. para o Brasil. Acta botanica Brasilica, 14(3), 263-265. [ Links ]
Campos, E. L., Sotão, H. M. P., Cavalcanti, M. A. Q., & Luz, A. B. (2005). Basidiomycetes de manguezais da APA de Algodoal-Maiandeua, Pará, Brasil. Boletim do Museu Paraense. Emílio Goeldi, 1(1), 97-102. [ Links ]
Cintrón, G. & Schaeffer-Novelly, Y. (1980). Introducción a la ecologia del manglar. São Paulo: Instituto Oceanográfico USP. [ Links ]
Clarke, K. R. & Warwick, R. M. (1994). Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory. [ Links ]
Deacon, J. W. (2006). Fungal biology (4th ed.). Massachusetts: Blackwell Publishing. [ Links ]
Drechsler-Santos, E. R., Santos, P. J. P., Gibertoni, T. B., & Cavalcanti, M. A. Q. (2010). Ecological aspects of Hymenochaetaceae in an area of Caatinga (semi-arid) in Northeast Brazil. Fungal Diversity, 42, 71-78. [ Links ]
Gibertoni, T. B., Santos, P. J. P., & Cavalcanti, M. A. Q. (2007). Ecological aspects of Aphyllophorales in the Atlantic Rain Forest in Northeast Brazil. Fungal Diversity, 25, 49-67. [ Links ]
Gibertoni, T. B. (2008). Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Scientifica Acta, 2, 70-74. [ Links ]
Gilbert, G. S. & Sousa, W. P. (2002). Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica, 34(3), 396-404. [ Links ]
Gilbert, G. S., Gorospe, J., & Ryvarden, L. (2008). Host and habitat preferences of polypore fungi in Microne- sian tropical flooded forests. Mycological Research, 112(6), 674-680. [ Links ]
Gilbertson, R. L. & Ryvarden, L. (1986). North American Polypores. (Vol. 1). Oslo: Fungiflora. [ Links ]
Gilbertson, R. L. & Ryvarden, L. (1987). North American Polypores. (Vol. 1). Oslo: Fungiflora. [ Links ]
Gugliotta, A. M. & Capelari, M. (1995). Polyporaceae from Ilha do Cardoso, SP, Brazil. Mycotaxon, 56, 107-113. [ Links ]
Hjortstam, K., Larsson, K. H., & Ryvarden, L. (1987). The Corticiaceae of North Europe. (Vol. 1). Oslo: Fungiflora. [ Links ]
Hjortstam, K., Larsson, K. H., & Ryvarden, L. (1988). The Corticiaceae of North Europe (Vol. 2). Oslo: Fungiflora. [ Links ]
Hyde, K. D. (1989). Ecology of tropical marine fungi. Hydrobiologia, 178, 199-208. [ Links ]
Kendrick, B. (2000). The fifth kingdom (2nd ed.). Newbury- port: Focus Information Group. [ Links ]
Lindblad, I. (2000). Host specificity of some wood-inha- biting fungi in a tropical forest. Mycologia, 92(3), 399-405. [ Links ]
Lindblad, I. (2001). Diversity of poroid and some corticoid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. Journal of Tropical Ecology, 17, 353-369. [ Links ]
Mendonça, I. V. S. & Almeida-Cortez, J. S. (2007). Caracterização da galha induzida por ácaro em Laguncularia racemosa (L.) Gaertn (Combretaceae). Biota Neotropica, 7(3), 163-170. [ Links ]
Montes, M. J. F., Macêdo S. J., & Koening, M. L. (2002). N: Si: P Atomic Ratio in the Santa Cruz Channel, Itamaracá- PE (Northeast Brazil): a Nyctemeral Variation. Brazilian. Archives of Biology and Technology, 45(2), 115-124. [ Links ]
Nogueira-Melo, G. S., Ryvarden, L., & Gibertoni, T. B. (2011). First record of Resupinatus poriaeformis (Agaricomycetes) from South America. Mycotaxon, 117, 423-427. [ Links ]
Nogueira-Melo, G. S., Medeiros, P. S., Gomes-Silva, A. C., Ryvarden, L., Sotão, H. M. P., & Gibertoni, T. B. (2012). Coriolopsis psila comb. nov. (Agaricomycetes) and two new Coriolopsis records for Brazil. Mycotaxon, 120, 223-230. [ Links ]
Núñez, M. & Ryvarden, L. (2000). East Asian Polypores Vol. 1. Ganodermataceae and Hymenochaetaceae. Synopsis Fungorum, 13, 1-168. [ Links ]
Núñez, M. & Ryvarden, L. (2001). East Asian Polypores. Vol. 2. Polporaceae sensu.lato. Synopsis Fungorum, 14, 169-522. [ Links ]
Peel, M. C., Finlayson, B. L., & McMahon, T. A. (2007). Updated world map of the K¨oppen-Geiger climate classification. Hydrology and Earth System Sciences, 11, 1633-1644. [ Links ]
Robledo, G. L., Urcelay, C., Domínguez, L., & Rajchenberg, M. (2006) Taxonomy, ecology and biogeography of polypores (Basidiomycetes) from Argentinian Polylepiswoodlands. Canadian Journal of Botany, 84, 1561-1572. [ Links ]
Robledo, G. L. & Renison, D. L. (2010). Wood-decaying polypores in the mountains of central Argentina in relation to Polylepis forest structure and altitude. Fungal Ecology, 3, 178-184. [ Links ]
Ryvarden, L. & Johansen, I. (1980). A preliminary polypore flora of East Africa. Oslo: Fungiflora. [ Links ]
Ryvarden, L. (1991). Genera of polypores, nomenclature and taxonomy. Synopsis Fungorum, 5, 1-363. [ Links ]
Schaeffer-Novelli, Y., Cintrón-Molero, G. R., Andaime, R., & Camargo, T. M. (1990). Variability of the Mangrove Ecosystems along the Brazilian coast. Estuaries, 13(2), 204-218. [ Links ]
Schnittler, M. & Stephenson, S. L. (2000). Myxomycete biodiversity in four different forest types in Costa Rica. Mycologia, 92(4), 626-637. [ Links ]
Silva, M. A. B., Bernini, E., & Carmo, T. M. S. (2005). Características estruturais de bosques de mangue do estuário do rio São Mateus, ES, Brasil. Acta Botanica Brasilica, 19(3), 465-471. [ Links ]
Sotão, H. M. P., Bononi, V. L. R., & Figueiredo, T. S. (1991). Basidiomycetes de manguezais da Ilha de Maracá, Amapá, Brasil. Boletim do Museu Paraense Emílio Goeldi, Série Botânica, 7(1), 109-114. [ Links ]
Trierveiler-Pereira, L., Santos P. J. P., & Baseia, I. G. (2013). Ecological aspects of epigeous gasteromycetes (Agaricomycetes, Basidiomycota) in four remnants of the Brazilian Atlantic Forest. Fungal Ecology, 6, 471-476. [ Links ]
Urcelay, C. & Robledo, G. (2004). Community structure of polypores (Basidiomycota) in Andean Alder wood in Argentina: Functional groups among wood-decay fungi? Austral Ecology, 29, 471-476. [ Links ]
Webster, J. & Weber, R. W. S. (2007). Introduction to Fungi. (3rd ed.). Cambridge: Cambridge University Press. [ Links ]
Yamashita, S., Hattori, T., Momose, K., Nakagawa, M., Aiba, M., & Nakashizuka, T. (2008). Effects of Forest Use on Aphyllophoraceous Fungal Community Structurein Sarawak, Malaysia. Biotropica, 40(3), 354-362. [ Links ]
1. Departamento de Micologia, Universidade Federal de Pernambuco, Av. Nelson Chaves s/n, CEP 50760-420, Recife, PE, Brazil; geomycota@gmail.com, tatiana.gibertoni@pq.cnpq.br
2. Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Nelson Chaves s/n, CEP 50760-420, Recife, PE, Brazil; pjp.santos@gmail.com
Received 12-XII-2013. Corrected 22-V-2014. Accepted 24-VI-2014.