Species richness and composition of epiphytic bryophytes in flooded forests of Caxiuanã National Forest, Eastern Amazon, BrazilABSTRACT
This study aimed to compare the richness and composition of the epiphytic bryoflora between várzea and igapó forests in Caxiuanã National Forest, Brazilian Amazon. Bryophytes were collected on 502 phorophytes of Virola surinamensis. Average richness per phorophyte and composition between forests and between dry and rainy periods was tested by two-way analysis and by cluster analysis, respectively. In total, 54 species of 13 families were identified. Richness was greater in igapó forest (44 species) compared to várzea forest (38 species). There was no significant difference in the number of species between the studied periods. Cluster analysis showed the bryoflora composition was different between várzea and igapó, but not between dry and rainy periods. Results did not corroborate the hypothesis that várzea forests harbor higher species richness than igapó forests.
Key words: Floristics; liverworts; mosses; seasonality
INTRODUCTION
Tropical rainforests are rich in epiphyte bryophytes due to high humidity levels (Richards 1954, 1984, Uniyal 1999, Germano and Pôrto 1998, Valente and Pôrto 2006, Santos and Costa 2008). One of the intrinsic characteristics of the Amazonian climate is the wide variation in its rainfall regime (Souza et al. 2009). In Amazonia, the richness of plant species, including epiphytes, is strongly correlated with absolute annual rainfall (Gentry 1988). The precipitation is one of the factors defining the floods in forests by white, black or light water rivers, called várzeas and igapós, both being representative in the Amazon biome (Prance 1979, Junk and Piedade 2005, Wittmann et al. 2006, Melack and Hess 2010, Junk et al. 2011).
Várzea forests are located on river margins and have Andean and pre-Andean origin, being associated with white water rivers, rich in nutrients with high concentration of sediments and dissolved minerals, as well as pH close to neutral. Igapó forests are also found on river banks, but have their origin from erosive resistant shields of Guiana and Central Brazil, being associated with black or light water rivers, poor in nutrients, with high amount of dilute organic matter, especially humic and fulvic acids, and an acid pH (Junk and Furch 1980).
Floristic and ecological studies in Amazonian floodable forests have mainly focused on trees (including palms) and lianas (Jardim and Vieira 2001, Wittmann et al. 2002, 2006, Carim et al. 2008, Ferreira et al. 2010, 2013, Lau and Jardim 2013, Montero et al. 2014), and vascular epiphytes (Quaresma and Jardim 2013, Medeiros et al. 2014, Travassos et al. 2014). Although floristic studies on non-vascular epiphytes of floodable forests in the Brazilian Amazon have already been performed by means of inventories (Lisboa et al. 1999, Ilkiu-Borges and Lisboa 2002, Moura et al. 2013) or comparative studies between vegetation formations (Ilkiu-Borges and Lisboa 2002, Santos and Lisboa 2003, Moraes 2006, Alvarenga and Lisboa 2009), studies comparing bryophyte richness and species composition among várzea and igapó forests are nonexistent.
Species richness from várzea and igapó forests varies depending on the organisms and/or region. Studies on arboreous groups and ferns in the two types of forests showed greater species richness in várzea forests, either in Central or Eastern Amazonia (Haugaasen and Peres 2006, Montero et al. 2014, Travassos et al. 2014). Opposite results, however, were found in Caxiuanã National Forest, where Virola surinamensis (Rol. ex Rottb.) Warb. (Myristicaceae), among other species, was reported as a common and frequent tree in both forest types (Ferreira et al. 2005, 2013).
Differences between plant groups in these two types of floodable forests are expected, since they are highly dynamic environments, with different geological ages and submitted to different nutrient regimes, as well as differences in luminosity and humidity (Junk et al. 2011, Ferreira et al. 2013). Variations in precipitation directly influence the moisture levels, which, in turn, support the development and reproduction of bryophytes, as they are plants with reproductive cycles dependent on the presence of water (Gentry 1988, Lisboa 1993).
The aim of this study was to compare the richness and species composition of epiphytic bryophytes on phorophytes of Virola surinamensis in floodable forests of Caxiuanã National Forest in two periods of precipitation (dry and rainy periods). Floristic and ecological knowledge of the bryophytes in these forests are essential in order to include it in the conservation strategies and management of the Amazonian biodiversity.
MATERIALS AND METHODS
Study area - Caxiuanã National Forest is located in the interfluve Xingu and Tocantins rivers, state of Pará, in the municipalities of Portel and Melgaço (01°42’30”S and 51°31’45”W; 62 m above sea-level). The annual average air temperature is 25.7 ± 0.8°C, the annual average relative air humidity is 82.3%. According to the Köppen climate classification, the climate is “Am” tropical wet climate and climate subtype with a short dry season (Oliveira et al. 2008). Precipitation from July 2013 to June 2014 in the Caxiuanã National Forest ranged from 65.3 to 324.11 mm, respectively (source: Projeto Estudo da Seca na Floresta - ESECAFLOR).
The Caxiuanã National Forest is predominantly composed by dense ombrophilous lowland forests or upland forests (85%), alluvial dense ombrophilous lowland forests or igapó and várzea forests (10%), enclaves of grassland, scrub vegetation, and patches of secondary vegetation resulting from human actions (Almeida et al. 2003).
Várzea forests in the Caxiuanã National Forest are seasonally flooded by annual and daily tidal fluctuations of main and small rivers and especially by the Caxiuanã Bay. Forest canopy is open and the understory is characterized by the presence, in natural regeneration, of individuals of arboreous species (Ferreira et al. 2013). The forests located near the Caxiuanã Bay are flooded by rivers with higher load of sediments and the soils are classified as Plinthosols, mineral soils formed under conditions of restriction of water percolation, submitted to the temporary effect of excess moisture. They are poorly drained and with greater proportion of nutrients (Piccini and Ruivo 2012).
Igapó forests are seasonally flooded by annual fluctuation of rivers and igarapés of black water and also by daily tidal flooding. This vegetation is characterized by having more closed canopy and dense vegetation in understory, with abundance of the herbaceous species Diplasia karatifolia Rich. and Calyptrocarya glomerulata (Brongn.) Urb., belonging to the family Cyperaceae, as well as representatives of Rapateaceae and Araceae (Ferreira et al. 2013, C.C. Souza et al., unpublished data). Soils are classified as Gleysols, presenting silty texture, with conditions of poor drainage and excessive regime of permanent or periodic moisture. They are poor in nutrients and with high fragility (Piccini and Ruivo 2012).
Data collection and identification - Collections were made on bark of Virola surinamensis (Rol.) Warb. located within the PELD plots (Pesquisas Ecológicas de Longa Duração - two plots in each forest) and surrounding areas in igapó (247 trees) and várzea (255 trees). Virola surinamensis was chosen due to its high density in both types of forest (Ferreira et al. 2005, 2013, C.C. Souza et al., unpublished data).
Sampling took place in two different periods, covering periods with lower and higher precipitation rates. Excursions occurred in July, September and November 2013 (precipitation of 65.3 mm, 35.1 mm and 119 mm, respectively) and in February, April and June 2014 (440 mm, 344 mm and 324 mm, respectively) (Table I).
Bryophyte samples were taken from phorophyte trunks in a standardized manner, using dimensions of 20 x 20 cm, as suggested by Frahm (2003), measured with a polystyrene frame.
Only phorophytes with diameter at breast height (DBH) above 20 cm were selected for sampling, which was always accomplished at a height of 1.30 m from the ground and face east. Sampling was performed independently, so new phorophytes were used in every collection, excluding the possibility of repetition of bryophyte collections on the same phorophyte.
Botanical material was identified with aid of keys in specialized literature, such as Gradstein and Costa (2003) and Gradstein and Ilkiu-Borges (2009). Adopted taxonomic classifications are in accordance with Goffinet et al. (2009) for Bryophyta and Crandall-Stotler et al. (2009) for Marchantiophyta. Botanical reference material was incorporated in the João Murça Pires Herbarium (MG) of the Museu Paraense Emílio Goeldi, and part of the material was donated to the Herbarium Rondoniensis of the Universidade Federal de Rondônia (UFRO).
Data Analysis - Based on the species occurrence number (Silva and Pôrto 2007, Pantoja et al. 2015) the absolute and relative frequencies of bryophytes were calculated for the two forest types. Comparison of the number of bryophyte species per phorophyte (dependent variable) in relation to forest type and the periods of lowest and highest precipitation (factors) was tested using a two-factor analysis of variance model, and the normality of the dependent variable was determined by the Shapiro-Wilk test (Zar 2010).
To verify the differences in the species composition between forest types and periods of lower and higher precipitation, a multivariate analysis of ordering (NMDS) was used, using the Sorensen similarity index and as a connecting measure the nearest neighbor (PC-ORD 4) (McCune and Mefford 1999).
RESULTS
In total 502 samples of bryophytes were analyzed, which correspond to 54 species of 13 families. The most representative family in both forest types was Lejeuneaceae, with 30 species, followed by Calymperaceae (5 spp.), Pylaisiadelphaceae (3 spp.), Plagiochilaceae (3 spp.), Fissidentaceae (2 spp.), Pilotrichaceae (2 spp.), Pterobryaceae (2 spp.), Sematophyllaceae (2 spp.), Hypnaceae, Leucobryaceae, Leucomiaceae, Neckeraceae, Radulaceae and Thuidiaceae (with one species each) (Table II).
Frequency of the bryophyte species in várzea and igapó forests during dry and rainy periods. R = rainy period; D = dry period; AF= absolute frequency; RF = relative frequency.
Species with the highest number of occurrences in várzea forest were Ceratolejeunea cubensis, Plagiochila montagnei, Radula javanica and Neckeropsis undulata, while the most frequent in igapó forest were Calymperes lonchophyllum, Ceratolejeunea cubensis, Prionolejeunea muricatoserrulata, Lejeunea cerina and Radula javanica.
Species richness was higher in igapó (44 spp.) than in várzea forest (38 spp.) (F[1,502] = 6.77; p = 0.01). However, there was no significant difference in species number in relation to periods with lower (dry period) and higher precipitation (rainy period), ranging from 33 to 31 species in várzea forests and from 36 to 35 in igapó forests, respectively (F[1,502 ] = 0.47; p = 0.493).
The ordering analysis showed the formation of two groups, and the first arrangement axis completely separates the species composition of epiphytic bryophyte community between the two types of forests, but there was no variation in species composition between dry and rainy periods (Fig. 1).
Distribution of species composition between igapó (i) and várzea (v) forests, and between dry (s) and rainy (c) periods.
DISCUSSION
The epiphytic bryoflora found in floodable forests in Caxiuanã National Forest in this study did not differ in species composition from other studies conducted in different forest types the Amazon region (Alvarenga and Lisboa 2009, Garcia et al. 2014, Tavares-Martins et al. 2014, Pantoja et al. 2015).
Regarding the distribution of species per families, the bryoflora of the studied floodable forests was consistent with what is known in tropical lowland forests, concerning the predominance of liverworts, especially because of the richness of Lejeuneaceae (Gradstein et al. 2001, Oliveira and Mota-de-Oliveira 2016). This has been a frequent result in studies with bryophytes performed in tropical forests in South America (Cornelissen and Gradstein 1990, Acebey et al. 2003, Gradstein and Costa 2003, Campelo and Pôrto 2007, Mota-de-Oliveira et al. 2009, Brito and Ilkiu-Borges 2014, Garcia et al. 2014, Tavares-Martins et al. 2014, Pantoja et al. 2015, Oliveira and Mota-de-Oliveira 2016). This family experienced recent periods of rapid diversification coinciding with the rise of the angiosperms in the Cretaceous (Feldberg et al. 2014, Bechteler et al. 2016), providing a wide morphological variation that allows them to develop in different environments, especially in tropical forests representing up to 70% of the bryoflora (Gradstein 1979, 1994, 1997, Gradstein et al. 2001).
Calymperaceae and Sematophyllaceae appear as most predominant among moss families in tropical rainforests, which coincide with the statement of Gradstein et al. (2001), and corroborate with further results from studies performed in the Amazon region (Lisboa et al. 1998, 1999, Santos and Lisboa 2003, Mota-de-Oliveira et al. 2009, Mota-de-Oliveira and ter Steege 2013, Brito and Ilkiu-Borges 2014, Garcia et al. 2014, Tavares-Martins et al. 2014, Pantoja et al. 2015).
Considering species frequencies, some bryophytes were found to be restricted to a single forest with a low number of occurrences. Harpalejeunea stricta, Pelekium scabrosulum and Isopterygium tenerum occurred exclusively in várzea forest. The first species is known from the understory to the higher zones of forest canopy (Tavares-Martins et al. 2014, Oliveira and Mota-de-Oliveira 2016), while Pelekium scabrosulum and Isopterygium tenerum occur in various types of vegetation, especially in humid and well-lit habitats (Moraes and Lisboa 2009, Florschütz-de-Waard 1986). Callicostella rufescens was, though, found only once in igapó forest. It has been commonly reported on trunks of living trees, decaying trunks and stones in tropical rainforests (Florschütz-de-Waard 1986).
Lopholejeunea subfusca and Mastigolejeunea auriculata are epiphytes preferring sunny environments, but were registered in the understory up to the canopy of different types of tropical forests (Gradstein 1994, Ilkiu-Borges and Lisboa 2002, Gradstein and Costa 2003, Mota-de-Oliveira and ter Steege 2013). In the present study, they were commonly found in the understory of várzea forest. It shows a displacement probably as the result of factors such as canopy openness (Acebey et al. 2003), characteristic of this type of forest, providing greater light-input.
Taxithelium planum, Taxithelium pluripuntactum, Trichosteleum papillosum, Octoblepharum cocuiense, Sematophyllum subsimplex, Fissidens prionodes and Fissidens guianensis are common species in upland forests, but a drastic reduction in their frequencies was noticed in floodable forests in this study, in which they had a maximum of five records. This reduction corroborates the data found by Moraes (2006) in várzea and igapó forests of Caxiuanã, and by Santos and Lisboa (2008) in northeastern Pará, when comparing bryophytes in different vegetation types.
Low frequency of these species has also been reported in a study conducted only in várzea forest (Moura et al. 2013), in which samples of various substrates were analyzed and the frequency of these species was consistent to that previously reported in flooded forests. In várzea and igapó forests of Caxiuanã, all these species had low frequency and this reduction was also observed in Octoblepharum albidum, Leucobryum martianum and Leucomium strumosum.
A wide variation in the species frequency among várzea and igapó forests was observed (Table II), such as Calymperes lonchophyllum colonizing a 177 phorophytes in igapó forest, but only 54 phorophytes in várzea forest. It is a species preferably found in living trunks and shady places (Reese 1993), which found better conditions to develop in the closed canopy of igapó forests. A similar correlation to várzea forest was observed on Plagiochila montagnei, which was present on 167 phorophytes in várzea and 13 in igapó. It had been reported occurring in canopy or understory of tropical forests, as well as in open vegetation, at low altitudes on living or decaying trunks and on rocks (Gradstein and Costa 2003, Gradstein and Ilkiu-Borges 2009).
These differences evidence how species behavior is apparently responding to conditions imposed by the environment, since even the most frequent species are presenting their reduced occurrences between environments, as well as the turnover of species from understory to canopy is best explained by microhabitat conditions in a forest instead of dispersion limitation (Mota-de-Oliveira et al. 2009).
Another factor contributing to these differences is the reproductive capacity of the species, since the bryophytes are plants with diverse reproductive strategies, which depend on the presence of water enabling the reproduction (Silva and Silva 2013). Low frequency of some species may be linked to their sexual system, for example, the dioecious species which have their fertilization rates affected by the spatial segregation between male and female colonies (Longton and Schuster 1983, Bowker et al. 2000, Oliveira and Pôrto 2002, Stark et al. 2005, 2010), as well as dioecious acrocarpous mosses, in which the sporophyte production rates in some families are very low (La Farge 1996).
As the low frequency, high frequency can also be associated with reproductive strategies of bryophytes, which reproduce not only sexually, but asexually as well (Löbel and Rydin 2009, Frey and Kürschner 2011, Maciel-Silva and Válio 2011, Maciel-Silva et al. 2013, Cerqueira et al. 2016). Various means of asexual reproduction represent a successful strategy allowing species to maintain the equilibrium between populations, given the difficulties imposed by the environment preventing sexual reproduction (Laaka-Lindberg 2000). Among epiphytic bryophytes, this strategy is widely adopted, especially by liverworts, as the colonization through new gemmae facilitates the establishment on vertical substrates (Glime 2007, Bastos 2008, Cerqueira et al. 2016). The lack of dispersion limitation among epiphytic bryophyte communities from Amazonian lowland forests indicated a predominance of niche-assembly rules over dispersal-assembly rules according to Mota-de-Oliveira et al. (2009).
The largest species richness of the epiphytic bryophyte community observed in igapó forests in comparison to várzea forests, is similar to the results of Ferreira et al. (2013) concerning the species richness of trees, lianas and stipes in these two forest types. However, these data contrast the results of Travassos et al. (2014), who showed species richness in várzea was twice that found in igapó forest.
In this study, it is believed that the difference in richness between the forests, being richer the igapó, is due to abundant presence of an herbaceous community (C.C. Souza et al., unpublished data), the presence of other types of substrates available for colonization (dead trunks, leaves), and the greater proximity between individuals of Virola surinamensis. Despite these phorophytes present a quite uniform distribution in both forest types, its occurrence is aggregated in igapó and dispersed in várzea (Ferreira et al. 2013). An aggregate distribution of phorophytes plus the fact that many bryophytes disperse their diaspores at short distances (Tan and Pócs 2000), may favor the eventual colonization by diaspores of bryophytes present on other phorophytes. Dispersion can also occur from diaspores of epiphyllous species present on herbaceous plants, and epixylic species, since the presence of dead trunks works as dispersion center to the colonization of living trunks (Wen-Zhang et al. 2009).
By choosing only one tree species widespread in várzea and igapó forests in Caxiuanã, characteristics relating to roughness of bark were not analyzed in this work, which seems to play a role in the establishment of bryophyte species (Gradstein and Culmsee 2010). However, a study by L.V. Ferreira et al. (unpublished data) about thickness of phorophytes, showed there is difference in the proportion of DBH of Virola surinamensis between igapó and várzea forests of Caxiuanã, where the igapó forest is characterized by having higher proportion of individuals presenting DBH from 10 to 20 cm, while the várzea forests have a greater proportion of individuals with larger DBH. Gradstein and Culmsee (2010) were the first to correlate trunk diameter with bryophyte diversity in species-rich tropical forest, which was previously shown only in temperate forests (McGee and Kimmerer 2002). According to Gradstein and Culmsee (2010), diameter of host trees correlated with distribution of few individual species, but not with community composition or species richness.
Trees with larger diameter and smoother barks seem to favor the development of bryophytes which grow more adherent to substrates, such as the members of Lejeuneaceae, as also observed by Bastos and Yano (2006) and those highlighted in these forests, including the four species recorded exclusively in várzea. However, in igapó forest, trees are thinner due to the low availability of nutrients (Schngart et al. 2005), but barks present more crevices and cracks. Such characteristics provide more microhabitats favoring water retention. They contribute to the development of species with growth forms producing mats on the substrate (Wen-Zhang et al. 2009), such as mosses, especially for members of Calymperaceae (Bastos 1999), which were more frequent in igapó, including eight species reported in this type of forest only.
Thus, it was found environmental action on the structure and distribution of phorophytes influences the epiphytic bryophyte community of understory and acts secondarily on its arrangement. More inclusion of phorophytes with detailed analysis of their cortex, researching along the vertical gradient, and monitoring for longer time of the lowest and highest precipitation periods, are strategies that can provide further details on the epiphytic bryoflora of floodable forests.
ACKNOWLEDGMENTS
The authors are grateful to Dr. Roberta Macedo Cerqueira and to the AABC reviewers for constructive comments on the manuscript; to Dr. Daniela Zappi for grammatically reviewing the manuscript; to the Programa de Pós-Graduação em Ciências Biológicas - Botânica Tropical of the Universidade Federal Rural da Amazônia (UFRA) and Museu Paraense Emílio Goeldi (MPEG) for the infrastructure and additional support; to the Ferreira Penna Research Station for the infrastructure and availability of field guide during the collections; to the Programa de Pesquisas Ecológicas de Longa Duração (PELD-Caxiuanã) for financing the field work; to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for granting scholarship to the first author; and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting productivity fellowship for the second and third authors.
REFERENCES
- ACEBEY A, GRADSTEIN SR AND KRÖMER T. 2003. Species richness and habitat diversification of bryophytes in submontane rain forest and fallows of Bolivia. J Trop Ecol 19: 9-18.
- ALMEIDA SS, AMARAL DD AND SILVA ASL. 2003. Inventário Florístico e Análise Fitossociológica dos Ambientes do Parque de Gumna, município de Santa Bárbara, Pará, Belém. Relatório Técnico Final do Mus Para Emílio Goeldi, Maio-2003, 117 p.
- ALVARENGA LDP AND LISBOA RCL. 2009. Contribution to the taxonomy, ecology and phytogeographical knowledge of Bryophytes from Eastern Amazonia. Acta Amaz 39: 495-504.
- BASTOS CJP. 2008. Vegetative reproduction patterns in species of Lejeuneaceae (Marchantiophyta) and its taxonomic and ecological significances Rev Bras Bot 31: 309-315.
- BASTOS CJP AND YANO O. 2006. Briófitas de Restinga das Regiões Metropolitana de Salvador e Litoral Norte do Estado da Bahia, Brasil. Bol Institut Bot (São Paulo) 18: 197-211.
- BECHTELER J, SCHÄFER-VERWIMP A, LEE GE, FELDBERG K, PÉRE-ESCOBAR OA, PÓCS T, PERALTA DF, RENNER MA AND HEIRINCHS J. 2016. Geographical structure, narrow species ranges, and Cenozoic diversification in a pantropical clade of epiphyllous leafy liverworts. Ecol Evol 7: 638-653.
- BOWKER MA, STARK LR, MCLETCHIE DN AND MISHLER BD. 2000. Sex expression, skewed sex ratios, and microhabitat distribution in the dioecious desert moss Syntrichia caninervis (Pottiaceae). Am J Bot 87: 517-526.
- BRITO ES AND ILKIU-BORGES AL. 2014. Bryophytes of an area of Terra Firme forest in the municipality of the Mirinzal and new records for the of Maranhão State, Brazil. Iheringia, Sér Bot 69: 133-142.
- CAMPELO MJA AND PÔRTO KC. 2007. A checklist of epiphyllous and epiphytic bryophytes from Frei Caneca RPPN, Jaqueira, Pernambuco State, Northeastern Brazil. Acta Bot Bras 21: 185-192.
- CARIM MJV, JARDIM MAG AND MEDEIROS TDS. 2008. Composição florística e estrutura de floresta de várzea no município de Mazagão, Estado do Amapá, Brasil. Sci For 36: 191-201.
- CERQUEIRA GR, ILKIU-BORGES AL AND FERREIRA LV. 2016. Seasonality of reproduction of epiphytic bryophytes in flooded forests from the Caxiuanã National Forest, Eastern Amazon. An Acad Bras Cienc 88: 903-910.
- CORNELISSEN JHC AND GRADSTEIN SR. 1990. On the ocurrence of bryophytes and macrolichens in different lowland rain forest types at Mabura Hill, Guyana. Trop Bryol 3: 29-35.
- CRANDALL-STOTLER B, STOTLER RE AND LONG DG. 2009. Morphology and classification of the Marchantiophyta. In: Goffinet B and Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge, Cambridge, p. 1-54.
- FELDBERG K, SCHNEIDER H, STADLER T, SCHÄFER-VERWIMP A, SCHMIDT AR AND HEINRICHS J. 2014. Epiphytic leafy liverworts diversified in angiosperm-dominated forests. Sci Rep 4: 5974.
- FERREIRA LV, ALMEIDA SS, AMARAL DD AND PAROLIN P. 2005. Riqueza e Composição de Espécies da Floresta de Igapó e Várzea da Estação Científica Ferreira Penna: Subsídios para o Plano de Manejo da Floresta Nacional de Caxiuanã. Pesquisas, Sér Bot 56: 103-116.
- FERREIRA LV, ALMEIDA SS AND PAROLIN P. 2010. Amazonian White- and Blackwater Floodplain Forests in Brazil: Large Differences on a Small Scale. Ecotro 16: 31-41.
- FERREIRA LV, CHAVES PP, CUNHA DA, MATOS DCL AND PAROLIN P. 2013. Variação da Riqueza e Composição de Espécies da Comunidade de Plantas entre as florestas de Igapós e Várzeas na Estação Científica Ferreira Penna-Caxiuanã na Amazônia Oriental. Pesquisas, Sér Bot 64: 175-195.
- FLORSCHÜTZ-DE-WAARD J. 1986. Musci (Part II). In: Stoffers AL and Lindeman JC (Eds), Flora of Suriname. E J Brill, Leiden, p. 273-361.
- FRAHM JP. 2003. Manual of Tropical Bryology. Trop Bryol, Duisburg.
- FREY W AND KÜRSCHNER H. 2011. Asexual reproduction, habitat colonization and habitat maintenance in bryophytes. Flor 206: 173-184.
- GARCIA ET, ILKIU-BORGES AL AND TAVARES-MARTINS ACC. 2014. Bryoflora of two terra-firme forests in the Área de Proteção Ambiental do Lago de Tucuruí, Pará State, Brazil. Hoehnea 41: 499-514.
- GENTRY AH. 1988. Changes in Plant Community Diversity and Floristic Composition on Environmental and Geographical Gradients. Ann Mo Bot Gard 75: 1-34.
- GERMANO SR AND PÔRTO KC. 1998. Briófitas Epíxilas de uma Área Remanescente de Floresta Atlântica (Timbaúba-PE, Brasil). Acta Bot Bras 3: 53-66.
-
GLIME JM. 2007. Bryophyte Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. http://www.bryoecol.mtu.edu/ Accessed November 14, 2014.
» http://www.bryoecol.mtu.edu - GOFFINET B, BUCK WR AND SHAW AJ. 2009. Morphology, anatomy, and classification of the Bryophyta. In: Goffinet B and Shaw AJ. Bryophyte Biology, 2nd ed., University Press Cambridge, Cambridge, p. 55-138.
- GRADSTEIN SR. 1979. The genera of the Lejeuneaceae: past and present. In: Clarke GCS and Duckett JG (Eds), Bryophyte systematics. Academic Press, London, p. 83-107.
- GRADSTEIN SR. 1994. Lejeuneaceae; Ptychantheae, Brachiolejeuneae. (Flora Neotropica Monograph 62). The New York Bot Gar Press, New York.
- GRADSTEIN SR. 1997. The Taxonomic Diversity of Epiphyllous Bryophytes. Abstr Bot 21: 15-19.
- GRADSTEIN SR, CHURCHILL SP AND SALAZAR-ALLEN N. 2001. Guide to the bryophytes of tropical America (Memoirs of the New York Botanical Garden, 86). The New York Bot Gar Press, New York.
- GRADSTEIN SR AND COSTA DP. 2003. The Hepaticae and Anthocerotae of Brazil (Memoirs of the New York Botanical Garden 87). The New York Bot Gar Press, New York.
- GRADSTEIN SR AND CULMSEE H. 2010. Bryophyte diversity on tree trunks in montane forests of Central Sulawesi, Indonesia. Trop Bryol 31: 95-105.
- GRADSTEIN SR AND ILKIU-BORGES AL. 2009. Guide to the Plants of Central French Guiana. Part 4. Liverworts and Hornworts. (Memoirs of the New York Botanical Garden 76). The New York Bot Gar Press, New York.
- HAUGAASEN T AND PERES CA. 2006. Floristic, edaphic and structural characteristics of flooded and unflooded forests in the lower Rio Purús region of central Amazonia, Brazil. Acta Amaz 36: 25-36.
- ILKIU-BORGES AL AND LISBOA RCL. 2002. Lejeuneaceae (Hepaticae). In: Lisboa PL (Org), Caxiuanã. Populações Tradicionais, Meio Físico e Diversidade Biológica. Mus Para Emílio Goeldi, Belém, p. 399-419.
- JARDIM MAG AND VIEIRA ICG. 2001. Composição e estrutura florística de uma floresta de várzea do estuário amazônico, ilha do Combu, Estado do Pará, Brasil. Bol Mus Para Emílio Goeldi Sér Bot 17: 333-354.
- JUNK WJ AND FURCH K. 1980. Water Chemistry and Aquatic Macrophytes of Rivers and Streams in Amazon River Basin and Adjacent Areas. Part I: Cuiabá - Porto Velho - Manaus. Acta Amaz 10: 611-633.
- JUNK WJ AND PIEDADE MTF. 2005. The Amazon River Basin. In: Fraser LH and Keddy PA (Eds), The World´s Largest Wet Lands: Ecology and Conservation. Cambridge University Press, Cambridge, p. 63-117.
- JUNK WJ, PIEDADE MTF, SCHÖNGART J, COHN-HAFT M, ADENEY MJ AND WITTMANN F. 2011. A Classification of Major Naturally-Occurring Amazonian Lowland Wetlands. Wetlands 31: 623-640.
- LA FARGE C. 1996. Growth Form, Branching Pattern, and Perichaetial Position in Mosses: Cladocarpy and Pleurocarpy Redefined. Bryol 99: 170-186.
- LAAKA-LINDBERG S. 2000. Substrate preference and reproduction in Lophozia silvicola (Hepaticopsida) in southern Finland. Ann Bot Fenn 37: 85-93.
- LAU AV AND JARDIM MAG. 2013. Florística e estrutura da comunidade arbórea em uma floresta de várzea na Área de Proteção Ambiental, Ilha do Combu, Belém, Pará. Bio Amaz 3: 88-93.
- LISBOA RCL. 1993. Musgos Acrocárpicos do Estado de Rondônia. Mus Para Emílio Goeldi, Belém.
- LISBOA RCL, LIMA MJL AND MACIEL UM. 1999. The Mosses of the Marajó Island - II - Municipallity of Anajá Pará, Brazil. Acta Amaz 29: 201-206.
- LISBOA RCL, MUNIZ ACM AND MACIEL UM. 1998. Moss from Marajó island, Brazil. III. Municpality of Chaves. Bol Mus Para Emílio Goeldi Sér Bot 14: 117-125.
- LÖBEL S AND RYDIN H. 2009. Dispersal and life history strategies in epiphyte metacommunities: alternative solutions to survival in patchy, dynamic landscapes. Oecologia 161: 569-579.
- LONGTON RE AND SCHUSTER RM. 1983. Reproductive biology. In: Schuster RM (Ed), New Manual of Bryology. Hattori Botanical Laboratory, Nichinan, p. 386-462.
- MACIEL-SILVA AS, COELHO MLP AND PÔRTO KC. 2013. Reproductive traits in the tropical moss Octoblepharum albidum Hedw. differ between rainforest and coastal sites. J Bryol 35: 206-215.
- MACIEL-SILVA AS AND VÁLIO IFM. 2011. Reproductive phenology of bryophytes in tropical rain forests: the sexes never sleep. Bryologist 114: 708-719.
- MCCUNE B AND MEFFORD MJ. 1999. PC-ORD version 4.0, multivariate analysis of ecological data, Users guide. MjM Sofware Design, Glaneden Beach, Oregon.
- MCGEE GG AND KIMMERER RW. 2002. Forest age and management effects on epiphytic bryophyte communities in Adirondack northern hardwood forests, New York, USA. Can J For Res 32: 1562-1576.
- MEDEIROS TDS, JARDIM MAG AND QUARESMA AC. 2014. Forófitos preferenciais de orquídeas epífitas na APA Ilha do Combu, Belém, Pará, Brasil. Bio Amaz 4: 1-4.
- MELACK JM AND HESS LL. 2010. Remote Sensing of the distribution and extent of wetlands in the Amazon Basin. In: Junk WJ et al. (Eds), Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management. Ecological Studies. Springer Verlag, Dordrecht-Heidelberg-London-New York, p. 44-58.
- MONTERO CJ, PIEDADE MTP AND WITTMANN F. 2014. Floristic variation across 600 km of inundation forest (Igapó) along the Negro River, Central Amazonia. Hydrobiologia 729: 229-246.
- MORAES ENR. 2006. Diversity, floristic and ecological aspects of Mosses (Bryophyta) Scientific Station Ferreira Penna, Flona Caxiuanã, Pará, Brazil. Dissertation, Federal Rural University of Amazon, Museu Paraense Emílio Goeldi. (Unpublished).
- MORAES ENR AND LISBOA RCL. 2009. Diversidade, taxonomia e distribuição por Estados brasileiros das famílias Bartramiaceae, Brachytheciaceae, Bryaceae, Calymperaceae, Fissidentaceae, Hypnaceae e Leucobryaceae (Bryophyta) da Estação Científica Ferreira Penna, Caxiuanã, Pará, Brasil. Acta Amaz 39: 773-792.
- MOTA-DE-OLIVEIRA S AND TER STEEGE H. 2013. Floristic overview of the epiphytic bryophytes of terra firme forests across the Amazon basin. Acta Bot Bras 27: 347-363.
- MOTA-DE-OLIVEIRA S, TER STEEGE H, CORNELISSEN JHC AND GRADSTEIN SR. 2009. Niche assembly of epiphytic bryophyte communities in the Guianas: a regional approach. J Biogeogr 36: 2076-2084.
- MOURA OS, ILKIU-BORGES AL AND BRITO ES. 2013. Bryoflora (Bryophyta and Marchantiophyta) of Combu Island, Belém, Pará State, Brazil. Hoehnea 40: 143-165.
- OLIVEIRA HC AND MOTA-DE-OLIVEIRA S. 2016. Vertical distribution of epiphytic bryophytes in Atlantic Forest fragments in northeastern Brazil. Acta Bot Bras 30: 609-617.
- OLIVEIRA LL, COSTA RF, SOUSA FAS, COSTA ACL AND BRAGA AP. 2008. Net precipitation and interception in Caxiuanã, in the Eastern Amazonia. Acta Amaz 38: 723-732.
- OLIVEIRA SM AND PÔRTO KC. 2002. Population Profile of Bryum apiculatum Schwaegr. in an Atlantic Forest Remnant, Pernambuco, Brazil. J Bryol 24: 251-258.
- PANTOJA ACC, ILKIU-BORGES AL, TAVARES-MARTINS ACC AND GARCIA ET. 2015. Bryophytes in fragments of terra firme forest on the great curve of the Xingu River, Pará State, Brazil. Xingu river and UHE Belo Monte environmental studies. Braz J Biol 75: 238-249.
- PICCININ J AND RUIVO ML. 2012. Os solos da Floresta Nacional de Caxiuanã. In: Plano de Manejo da Floresta Nacional de Caxiuanã. 1: 120-127.
- PRANCE GT. 1979. Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subject to inundation. Brittonia 31: 26-38.
- QUARESMA AC AND JARDIM MAG. 2013. Phytosociology and spatial distribution of epiphytic bromeliads in Amazon estuarine floodplain forest. Braz J Biosc 11: 1-6.
- REESE WD. 1993. Calymperaceae (Flora Neotropica 58). The New York Botanical Garden Press, New York.
- RICHARDS PW. 1954. Notes on the bryophytes communities of lowland tropical rainforest with special reference to moraballi creek, British Guiana. Vegetatio 5: 319-328.
- RICHARDS PW. 1984. The Ecology of tropical forest bryophytes. In: Schuster RM (Ed), New Manual of Bryology. Hattori Botanical Laboratory 2, Nichinan, Japan, p. 1233-1269.
- SANTOS ND AND COSTA DP. 2008. The importance of Private Natural Heritage Reserves for conservation of Atlantic rain forest bryoflora: a study at El Nagual, Magé, Rio de Janeiro State, Brazil. Acta Bot Bras 22: 359-372.
- SANTOS RC AND LISBOA RCL. 2003. Mosses (Bryophyta) of northeast Pará, Brazil - 1. Zona Bragantina Salgado Microregion and Viseu Municipality. Acta Amaz 33: 415-422.
- SANTOS RC AND LISBOA RCL. 2008. Mosses (Bryophyta) of the micro-region of Salgado Paraense and its use as possible indicators of disturbed ambiente. Rodriguésia 59: 361-368.
- SCHÖNGART J, PIEDADE MT, WITTMANN F, JUNK WJ AND WORBES M. 2005. Wood growth patterns of Macrolobium acaciifolium (Benth.) Benth. (Fabaceae) in Amazonian black-water and white-water floodplain forests. Oecologia 145: 654-661.
- SILVA LTP AND SILVA AG. 2013. Breeding systems in Bryophytes: small plants of high reproductive success. Natureza online 11: 155-160.
- SILVA MPP AND PÔRTO KC. 2007. Composição e riqueza de briófitas epíxilas em fragmentos florestais da Estação Ecológica de Murici, Alagoas. Braz J Biosc 5: 243-245.
- SOUZA EB ET AL. 2009. Seasonal precipitation in eastern Amazon during rainy season: regional observations and RegCM3 simulations. Rev Bras Meteorol 24: 111-124.
- STARK LR, MCLETCHIE DN AND EPPLEY SM. 2010. Sex ratios and the shy male hypothesis in the moss Bryum argenteum (Bryaceae). Bryologist 113: 788-797.
- STARK LR, MCLETCHIE DN AND MISHLER BD. 2005. Sex expression, plant size, and spatial segregation of the sexes across a stress gradient in the desert moss Syntrichia caninervis. Bryologist 108: 183-193.
- TAN BC AND PÓCS T. 2000. Bryogeography and conservation of bryophytes. In: Shaw AJ and Goffinet B. Bryophyte biology, v1. University Press Cambridge, Cambridge, p. 403-476.
- TAVARES-MARTINS ACC, LISBOA RCL AND COSTA DP. 2014. Bryophyte flora in upland forests at different successional stages and in the various strata of host trees in northeastern Pará, Brazil. Acta Bot Bras 28: 46-58.
- TRAVASSOS CC, JARDIM MAG AND MACIEL S. 2014. Floristics and ecology of ferns and lycophytes as indicators of environmental conservation. Bio Amaz 4: 40-44.
- UNIYAL PL. 1999. Role of Bryophytes in Conservation of Ecossystems and Biodiversity. The Botanica 49: 101-115.
- VALENTE EB AND PÔRTO KC. 2006. Hepatics (Marchantiophyta) from a fragment of Atlantic Forest in Serra da Jibóia, in the Municipality of Santa Teresinha, Bahia State, Brazil. Acta Bot Bras, p. 433-441.
- WEN-ZHANG M, WEN-YAO L AND XING-YANG L. 2009. Species composition and life forms of epiphytic bryophytes in old - growth and secondary forests in Mt. Ailao, SW China. Cryptogam Bryol 30: 477-500.
- WITTMANN F, ANHUF D AND JUNK WJ. 2002. Tree species distribution and community structure of central amazonian várzea forests by remote-sensing techniques. J Trop Ecol 18: 805-820.
- WITTMANN F, SCHÖNGART J, MONTERO JC, MOTZER T, JUNK WJ, PIEDADE MTF, QUEIROZ HL AND WORBES M. 2006. Tree species composition and diversity gradients in white-water forest across the Amazon basis. J Biogeogr 33: 1334-1347.
- ZAR JH. 2010. Biostatistical Analysis. 5th ed., Pearson Prentice-Hall, Upper Saddle River, New Jersey.
Publication Dates
-
Publication in this collection
16 Oct 2017 -
Date of issue
2017
History
-
Received
12 Dec 2016 -
Accepted
29 June 2017
