Three typical mangrove tree species were frequently found in the study areas: Avicennia schaueriana Stapf. and Leech (black mangrove), 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 eight months (Apr, May, Jun, Jul, Aug, Sep, 2009; Jan and Mar 2010), totaling 32 field trips (16 along each coast).

All basidiomata found along transects were placed in paper bags and collection data (position, date and substrate) was recorded. The material was air-dried and identified with help of existing literature (Ryvarden & Johansen, 1980; Gilbertson & Ryvarden, 1986; 1987; Hjortstam, Larsson & Ryvarden, 1987; 1988; Ryvarden, 1991; Boidin, Lanquetin & Gilles, 1997; Boidin & Gilles, 2000; Núñez & Ryvarden, 2000; 2001; Ryvarden, 2004; Bernicchia, 2005). Nomenclature from the CABI online database (www.indexfungorum.org) was used. Identified material in good condition was incorporated into the URM Herbarium, of the Department of Mycology of the Universidade Federal de Pernambuco, and duplicates were sent to the O Herbarium of the University of Oslo. Samples of the same species collected in the same area in the same substrate and on the same date were identified as one combined voucher specimen.

Species abundance values were represented by the number of occurrences of specimens/individuals in each substrate per transect (ind./10 000m2). 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 analysis (ANOVA) was used to determine significant differences for abundance and richness between both mangroves and precipitation periods (dry and wet), and two-way similarity analysis (ANOSIM) was used to determine significant differences in the macrofungi community structure between the four mangroves and sampling seasons. Bartlett’s test was used to determine the homogeneity of variances and values were transformed into Neperian logarithms if necessary.

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 probability distribution was used to evaluate spatial distribution and verify if there was predominance of some fungal species in any of the mangroves. Species considered not to be rare were used in the analysis and the areas were tested separately. In the present study, rare species were those whose frequency of occurrence was 0.5<F≤1.5%, using the formula: F=n×100/N, where n=number of specimens from one species and N=total number of specimens (Lindblad, 2000; Schnittler & Stephenson, 2000). The probability value used (P) was that of species with higher incidence (Ayres, Ayres, Ayres & Santos, 2007).

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 for this analysis. If not stated, the level of significance was set at p<0.05 for all other analyses.

Abiotic factors considered in this study were temperature and rainfall, data of which was provided by the Instituto de Tecnologia de Pernambuco - ITEP/Agência Pernambucana de Água e Clima (APAC). Dry months (Sep 2009, Jan and Mar 2010) were considered those in which the total value of precipitation was below the lower limit of the confidence interval (95%) for the average annual monthly precipitation over the last 10 years.

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 striatum; 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 collected specimens, 81 occurred in S, 66 in T, 73 in M and 55 in A. The Santa Cruz Chanel presented the highest number of genera and species (18 and 20, respectively), followed by T (15 genera, 16 species), M (12, 16) and A (12, 13). Although richness and abundance varied, they did not differ significantly between areas [F(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, p=0.001) (Fig. 1).

Of the 33 species, four were common to all four areas: G. striatum, P. gilvus, S. paradoxa and T. biforme. Significantly different rates of occurrence according to area were found for nine of the 11 fungal species (82%) which were sufficiently abundant for statistical testing (Table 2, in bold). Coriolopsis hostmanii, P. gilvus and T. biforme were predominant in S; 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. detrita 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 rainfall in the four areas from April 2009 to March 2010 was 174.13mm, varying monthly from 0mm to 543.2mm. The mean temperature was 25.17°C. The driest month was October (11.6mm) and the wettest month was April (409.85mm). January, February, March, September, October, November and December were considered to be the dry season, while April, May, June, July and August represented the rainy season (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 [F(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 (Rglobal=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 0.33, respectively), according to Clarke & Warwick (1994), genuinely different communities would result in Rglobal values above 0.5.

Furthermore, in transects of the Northern mangroves, A. schaueriana was predominant, while R. mangle was predominant in transects of the Southern mangroves. In estuaries, salinity and/or proximity to the sea influenced the distribution of mangrove plant species (Cintrón & Schaeffer-Novelli, 1980; Schaeffer-Novelli et al., 1990). Additionally, the Northern mangroves were surrounded by urban areas, while the Southern mangroves were distant from such areas (Montes et al., 2002; Mendonça & Almeida-Cortez, 2007), and thus have less antropic impacts. Hyde (1989) described the negative effects of hydrocarbon spillage on microfungi diversity in mangroves in Brunei, while Yamashita et al. (2008) described the negative effects of agriculture and isolated patches of natural forest on aphyllophoraceous diversity in Malaysia. However, the hypothesis that anthropization influences fungal communities was not tested in the present work. Hence, the distribution of the fungal species may reflect the vegetation in the studied transects.

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 also been reported in other ecosystems in Brazil. Gibertoni et al. (2007) observed that the former aphyllophoroid fungi were more frequently collected in the dry season, after peaks of rainfall in the Atlantic Forest. In Amazonia, Gibertoni (2008) found that the composition of polyporoid fungi species was different in the rainy than in the dry season. This indicates that rainfall is a factor that influences the occurrence of species and specimens.

However, Drechsler-Santos et al. (2010) observed in caatinga (semi-arid region), that rainfall did not influence the occurrence of species of Hymenochaetaceae, mostly found in living hosts. This is probably because they do not depend on environmental humidity as they are adapted to moisture hosts, according to Boddy & Rayner (1983).

Recently, Trierveiler-Pereira et al. (2013) reported no significant differences in composition and species richness of epigeous Gasteromycetes according to collecting seasons in the Atlantic Forest, probably due to ephemeral basidiomata, which may not be observed, even during the rainy season.

The results of the present study support the tested hypothesis that diversity of macrofungi occurring in mangroves is directly affected by both rainfall and area of collection. We recommend further studies should collect samples during the higher precipitation months and from transects dominated by different mangrove plants in the same area in order to identify the overall diversity of the mycobiota in this ecosystem.

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 Científico e Tecnológico (CNPq, master scholarship of GSNM) and by FACEPE (APQ 0444-2.03/08).

RESUMEN

La estructura de la comunidad de basidiomicetos macroscópicos (Fungi) en los manglares brasileños influenciada por las variaciones temporales y espaciales. 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 plantas de manglar en el mismo ecosistema son deseables para acceder a la diversidad de la micobiota.

Palabras clave: Agaricomycetes, diversidad, interacciones ecológicas, estuarios, hongos.

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