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Composition and structure of the bryophyte community of Park Savanna in Marajó Island, Pará, Brazil

Abstract

Aiming to enrich the knowledge about the flora of savannas, this paper studied the composition and structure of the bryophyte community of Park Savanna areas in Marajó Island - PA. Biological material was collected within 60 100-m2 plots equally distributed in the dry season of 2016 and the rainy season of 2017 in five Park Savanna areas (SP-I to SP-V). The composition, density, richness and diversity of species and presence of indicator species were compared between the sampled areas and seasons. The species were classified according to the substrates colonized and ecological groups of light tolerance. Significant differences in SP-V indicated that the area was the main factor influencing the composition of bryophytes (p: 0.0001), with five indicator species. There were also significant differences in density (p = 0.0001168) and richness (p = 0.0001317) of bryophytes between seasons (p-value = 0.3393; p-value = 0.04065; p: 0.1081). There was a predominance of generalist (25 spp.) and corticolous (728 individuals) species, which were widely distributed in the sampled areas. Therefore, the structure of the bryophyte communities was not influenced by seasonality, and this indicates that these plants are adapted to the environmental conditions.

Key words
amazonian savannas; bryoflora; ecology; seasonal precipitation

INTRODUCTION

Brazilian savannas (Cerrado) are predominantly distributed in the Central Plateau region, forming the second largest neotropical biome and considered one of the biodiversity hotspots for conservation priorities (Myers et al. 2000MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GAB & KENT J. 2000. Biodiversity hotspots for conservation priorities. Nat 403: 853-858., Rios et al. 2016RIOS ABM, OLIVEIRA JPS, SILVA RP, OLIVEIRA-NETO JF, OLIVEIRA LS, PERALTA DF & MACCAGNAN DHB. 2016. Bryophyte diversity in an area of Brazilian Cerrado in Central-West. Neotrop Biol Conserv 11: 132-140.). Savannas also occur within the Amazon biome (Amazonian savannas) formed by disjoint patches that altogether cover an area of ​​about 267 km2 (Carvalho & Mustin 2017CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahhs. Nat Ecol Evol 1: 1-3.). They reach the east portion of the Marajó island and other spots distributed in the states of Amapá, Amazonas, Pará and Roraima (Prance 1996PRANCE GT. 1996. Islands in Amazonia. Philos Trans Royal Soc/London 351: 823-833., Rossetti et al. 2007ROSSETTI DF, VALERIANO MM & THALLÊS M. 2007. An abandoned estuary within Marajó Insland: implications for late quaternary paleogeography of northern Brazil. Estuar Coasts 30: 813-826.), and are characterized by the predominance of grasses and a variable density of trees and shrubs (Silva & Oliveira 2018SILVA GFN & OLIVEIRA IJ. 2018. Reconfiguração da paisagem nas savanas da Amazônia. Mercator 17: 1-20.).

Savannas are ecosystems influenced by high light intensity and drought events, which increase the chances of spread of fires (Hoffmann et al. 2012HOFFMANN WA, JACONIS S, MCKINLEY K, GEIGER E, GOTSH S & FRANCO AC. 2012. Fuels or microclimate? Understanding the drivers of fire feedbacks at savannah forest boundaries. Aust Ecol 37: 634-643.). Microclimatic conditions such as luminosity, temperature, humidity, and pH act as environmental filters that can determine the structure of bryophyte communities (Weibull & Rydin 2005WEIBULL H & RYDIN H. 2005. Bryophyte species richness on boulders: Relationship to area, habitat diversity and canopy tree species. Biol Conserv 122: 71-79., Bello et al. 2010BELLO F ET AL. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiver Conserv 19: 2873-2893., Smith & Stark 2014SMITH RJ & STARK LR. 2014. Habitat vs. dispersal constraints on bryophyte diversity in the Mojave Desert, USA. J Arid Environ 102: 76-81., Santos et al. 2014SANTOS ND, COSTA DP, KINOSHITA LS & SHEPHERD GJ. 2014. Windborne: Can liverworts be used as indicators of altitudinal gradient in the Brazilian Atlantic Forest? Ecol Indicators 36: 431-440.). Desiccation tolerant bryophytes are common in savannas (Visnadi & Vital 1989VISNADI SR & VITAL DM. 1989. Briófitas rupícolas de um trecho do rio Bethary, Iporanga, estado de São Paulo. Acta Bot Bras 3: 179-183.), since only the best adapted species settle in these areas (Kürschner 2004KÜRSCHNER H. 2004. Life strategies and adaptations in bryophytes from the nearand Middle east. Turkish J Bot 28: 73-84., Kürschner & Parolly 2005KÜRSCHNER H & PAROLLY G. 2005. Ecosociological studies in Ecuadorian bryophyte communities III. Life forms, life strategies and ecomorphology of the submontane and montane epiphytic vegetation of S Ecuador. Nova Hedwigia 80: 89-113., Pardow & Lakatos 2013PARDOW A & LAKATOS M. 2013. Desiccation tolerance and global change: implications for tropical bryophytes in lowland forests. Biotropica 45: 27-36.).

The composition of bryophytes in tropical forest is influenced by microhabitat variability along the different height zones of host trees (Holz et al. 2002HOLZ I, GRADSTEIN SR, HEINRICHS J & KAPPELLE M. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105: 334-348., Gosselin et al. 2017GOSSELIN M, FOURCIN D, DUMAS Y, GOSSELIN F, KORBOULEWSKY N, TOÏGO M & VALLET P. 2017. Influence of forest tree species composition on bryophytic diversity in mixed and pure pine (Pinus sylvestris L.) and oak (Quercus petraea (Matt.) Liebl.) stands. For Ecol Manage 406: 318-329.). The relationship of bryophytes with the microhabitat can be explained by structural and chemical characteristics of the substrate and exposure to light, wind and precipitation (Hespanhol et al. 2011HESPANHOL H, SÉNECAA A, FIGUEIRA R & SÉRGIO C. 2011. Microhabitat effects on bryophyte species richness and community distribution on exposed rock outcrops in Portugal. Plant Ecol Divers 4: 251-264., Gosselin et al. 2017GOSSELIN M, FOURCIN D, DUMAS Y, GOSSELIN F, KORBOULEWSKY N, TOÏGO M & VALLET P. 2017. Influence of forest tree species composition on bryophytic diversity in mixed and pure pine (Pinus sylvestris L.) and oak (Quercus petraea (Matt.) Liebl.) stands. For Ecol Manage 406: 318-329.).

The distribution pattern of plant communities in Amazonian savannas is still little known (Cavalcante et al. 2014CAVALCANTE CO, FLORES AS & BARBOSA RI. 2014. Fatores edáficos determinando a ocorrência de leguminosas herbáceas em savanas amazônicas. Acta Amaz 44: 379-386.) and more studies are needed to promote the conservation of their biodiversity, which has a high rate of endemic species (Strassburg et al. 2017STRASSBURG BBN ET AL. 2017. Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1: 0099.). Many of these species in Amazonian savannas are threatened with extinction due to constant clearance of forest areas to meet agriculture and livestock demands associated with population growth (Plotkin & Riding 2011PLOTKIN RL & RIDING S. 2011. Biogeography of the Llanos de Moxos: natural and anthropogenic determinants. Biogeogr Llanos Moxos 66: 183-192., Carvalho & Mustin 2017CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahhs. Nat Ecol Evol 1: 1-3.).

In view of the heterogeneity and social value of their different phytophysiognomies of savannas (Plotkin & Riding 2011PLOTKIN RL & RIDING S. 2011. Biogeography of the Llanos de Moxos: natural and anthropogenic determinants. Biogeogr Llanos Moxos 66: 183-192., Fearnside 2015FEARNSIDE PM. 2015. Pesquisa sobre conservação na Amazônia brasileira e a sua contribuição para a manutenção da biodiversidade e uso sustentável das florestas tropicais. In: Vieira I, Jardim M & Rocha E. Amazônia em Tempo: Estudos Climáticos e Socioambientais. Universidade Federal do Pará, Museu Paraense Emílio Goeldi and Embrapa Amazônia Oriental, Belém, p. 21-49.), their conservation requires investments in research for the implementation of new Environmental Protection Areas (Mustin et al. 2017MUSTIN K ET AL. 2017. Biodiversity, threats and conservation challenges in the Cerrado of Amapá, an Amazonian savana. Nat Conserv 22: 107-127.). Knowledge of the ecology of bryophytes can be useful because these plants can serve as models for management and conservation strategies of these savannas. Since, some studies simulating environmental changes and micro fossil analyses have suggested that climate change will strongly affect both the abundance and composition of the briophyte communities (Dorrepaal et al. 2004DORREPAAL E, AERTS R, CORNELISSEN JHC, CALLAGHAN TV & VAN LOGTESTIJN RSP. 2004. Summer warming and increased winter snow cover affect Sphagnum fuscum growth, structure and production in a sub-arctic bog. Glob Change Biol 10: 93-104., Walker et al. 2006WALKER MD ET AL. 2006. Plantcommunity responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103: 1342-1346., Lang et al. 2009LANG SI, CORNELISSEN JHC, HOELZER A, TER BRAAK CJF, AHRENS M, CALLAGHAN TV & AERTS R. 2009. Determinants of cryptogam composition and diversity inSphagnum-dominated peatlands: the importance of temporal, spatial andfunctional scales. J Ecol 97: 299-310., Elmendorf et al. 2012ELMENDORF SC ET AL. 2012. Global assessment ofexperimental climate warming on tundra vegetation: heterogeneity overspace and time. Ecol Lett 15: 164-175.), which in turn affects the structure and functioning of the ecosystem where bryophytes and vascular plants cooccur (He et al. 2016HE X, HEB KS & HYVÖNEN J. 2016. Will bryophytes survive in a warming world? PERSPECT Plant Ecol 19: 49-60.).

The objective of the present study was to evaluate the composition and structure of bryophyte communities in Park Savanna areas in Marajó Island, state of Pará.

MATERIALS AND METHODS

Study area

The study area corresponded to five savannas classified as belonging to the Park Savanna (SP) phytophysiognomy (Rossetti et al. 2007ROSSETTI DF, VALERIANO MM & THALLÊS M. 2007. An abandoned estuary within Marajó Insland: implications for late quaternary paleogeography of northern Brazil. Estuar Coasts 30: 813-826., IBGE 2012IBGE. 2012. Manual Técnico da Vegetação Brasileira. 2nd ed., Rio de Janeiro: Departamento de Recursos Naturais e Estudos Ambientais, 271 p.), located in the east side of the Marajó Island, state of Pará. Four Park Savanna areas are located in the municipality of Salvaterra; of these, SP-I (00° 47’ 47.5’’ S and 48° 32’ 39.7’’ W) and SP-IV (00° 52’ 24.8’’ S and 48° 35’ 07.7’’ W) can be easily seen from the Camará-Salvaterra road margins, and SP-II (00° 51’ 44,4” S and 48° 31’ 45,0” W) and SP-III (00° 51’ 09,4’’ S and 48° 31’ 55,9” W) from the Salvaterra-Joanes road. The SP-V (00° 54’ 32.3’’ S and 48° 40’ 06.9” W) is located at the margins of the PA-154 road, in the municipality of Cachoeira do Arari. The peculiar characteristics of the current physiognomic aspect of these savannas are described in Table I. The climate is humid equatorial with average annual temperature of 28°C and precipitation all the year round. The months with less precipitation in the period studied were August through October (average of 19 mm) and the ones with more precipitation were January through April (average of 504 mm). This information was obtained from the database of the National Institute of Meteorology (http://www.inmet.gov.br/portal/index.php?r = home2/index).

Table I
Phytophysiognomy characterization of the five Park Savanna areas in Marajó Island, Pará, Brazil.

Sampling, collection and taxonomic identification

Sixty 100 m2 (10 m x 10 m) plots were established and usual sampling techniques for bryophytes were adopted (Vanderpoorten et al. 2010VANDERPOORTEN A, PAPP B & GRADSTEIN R. 2010. Sampling of bryophytes. In: Eyman J, Degreef J, Häuser C, Monje, JC, Samyn Y & Vanden-Spiegel D (Eds), Manual on field recording techniques and protocols for All Taxa Biodiversity Inventories and Monitoring. ABC Taxa 8: 340-354.). Thirty plots were equally distributed in the five savannas during the dry season of 2016, and 30 during the rainy season in 2017. Field collection and preservation of botanical material followed the methodology of Glime (2017)GLIME JM. 2017. Field Taxonomy and Collection Methods. Chapt. 1. In: Glime JM (Ed), Bryophyte Ecology. V. 3. Methods. Ebook Michigan Technological University and the International Association of Bryologists, 20 p.. The bryophytes were collected in wooden paper bags and a single bag corresponded to a sample, which in this study was adopted the theme occurrence to represent the species found in each sample. Within each plot, it had at least five living trees, where the bryophytes were collected from the base to the crown of host trees (accessed through climbing techniques), but without dividing crown into zones. In some plots, bryophytes were also collected in decomposing trunks, soil, and termite mounds. Specialized literature (Buck 2003BUCK WR. 2003. Guide to the Plants of Central French Guiana. Part 3. Mosses. (Memoirs of the New York Botanical Garden 76). The New York Bot Gar Press, New York., Florschütz-De Waard 1996FLORSCHÜTZ-DE WAARD J. 1996. Sematophyllaceae. Musci III. In: Görts-Van Rijn ARA (Ed), Flora of the Guianas. Series C: Bryophytes Fascicle 1: 439-462., Gradstein & Ilkiu-Borges 2009GRADSTEIN SR & 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.) was used for identification and the classification system adopted was the one of Crandall-Stotler et al. (2009)CRANDALL-STOTLER B, STOTLER RE & LONG DG. 2009. Morphology and classification of the Marchantiophyta. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge, Cambridge, p. 1-54. for liverworts and Goffinet et al. (2009)GOFFINET B, BUCK WR & SHAW AJ. 2009. Morphology, anatomy, and classification of the Bryophyta. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge: Cambridge, p. 55-138. for mosses. The database of the Flora do Brasil 2020 under construction (Costa & Peralta 2015COSTA DP & PERALTA DF. 2015. Bryophytes diversity in Brazil. Rodriguésia 66(4): 1-9.) was used to confirm scientific names. The botanical material was incorporated in the Prof. Dr. Marlene Freitas da Silva (MFS) Herbarium of the State University of Pará.

Data analysis

Species accumulation curves were generated in the iNEXT software (Hsieh et al. 2013HSIEH TC, MA KH & CHAO A. 2013. iNEXT online: interpolation and extrapolation (Version 1.0) [Software]. Available in: http://chao.stat.nthu.edu.tw/blog/software-download/.
http://chao.stat.nthu.edu.tw/blog/softwa...
), using an individual based data matrix of the bryophyte communities to evaluate sampling sufficiency.

The composition of the community was compared between the two seasons and between areas through PERMANOVAs based on a Bray-Curtis distance matrix (Zar 2010ZAR JH. 2010. Biostatistical Analysis. 5th ed., Pearson Prentice-Hall, Upper Saddle River, New Jersey.) and summarized through a Principal Component Analysis (PCA). Indicator species analysis (IndVal), carried out in the R software (Dufrêne & Legendre 1997DUFRÊNE M & LEGENDRE P. 1997. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecol 67: 345-366.), was used to identify whether some of the species could indicate differences in composition. Mean values of density, richness and diversity per plot were adopted to analyze the structure of the community. The Student’s t-test (or the non-parametric equivalent test) was used to compare the density and richness between seasons, and the Kruskal-Wallis rank-sum test (Dunn 1964DUNN OJ. 1964. Multiple comparisons using rank sums. Technometrics 6: 241-252.) was used for pairwise multiple comparisons between areas. Two-way Analysis of Variance (ANOVA) was used to compare the density and richness of bryophytes between different areas in the two seasons (Ayres et al. 2007AYRES M, AYRES-ÚNIOR M, AYRES DL & SANTOS AA. 2007. BIOESTAT - Aplicações estatísticas nas áreas das Ciências Bio-Médicas. Belém: Mamirauá, 364 p.). The interaction plot (interaction plot) was used to facilitate the interpretation of the boxplot generated in the two-way ANOVA. The Fisher’s alpha diversity index (Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. New Jersey: Princeton University Press, Princeton.) was used to analyze the variations of species richness and abundance between seasons and areas sampled, using the “vegan” package (Oksanen et al. 2007OKSANEN J, KINDT R, LEGENDRE P, O’HARA B, HENRY M & STEVENS H. 2007. Vegan: Community Ecology Package. R package, version 1.8-8. 2007. Available in: http://cran.r-project.org/, http://r-forge.r-project.org/ projects/vegan/.
http://cran.r-project.org/, http://r-for...
) in the R software v. 3.1.3 (R Development Core Team 2018R CORE TEAM. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: https://cran.r-project.org/bin/windows/base/old/3.1.3/.
https://cran.r-project.org/bin/windows/b...
).

For the study of species distribution, the species were classified according to the ecological groups of light tolerance, namely, sun specialists, shade specialists, and generalists. This classification was based on the works of Richards (1984)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., Gradstein et al. (2001)GRADSTEIN SR, CHURCHILL SP & 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., Pantoja et al. (2015)PANTOJA ACC, ILKIU-BORGES AL, TAVARES-MARTINS ACC & GARCIA ET. 2015. Bryophytes in fragments of Terra Firme forest on the great curve of the Xingu River, Pará state, Brazil. Braz J Biol 75: 238-249., and Fagundes et al. (2016)FAGUNDES DN, TAVARES-MARTINS AC, ILKIU-BORGES AL, MORAES ER & SANTOS RCP. 2016. Riqueza e aspectos ecológicos das comunidades de briófitas (Bryophyta e Marchantiophyta) de um fragmento de Floresta de Terra Firme no Parque Ecológico de Gunma, Pará, Brasil. Iheringia, Sér Bot 71: 72-84.. To verify whether there were specific communities in the different areas or if there was a single community of generalist species throughout the savannas, the density and richness of generalist species was analyzed by multiple comparisons with the Kruskal-Wallis rank-sum test (Dunn 1964DUNN OJ. 1964. Multiple comparisons using rank sums. Technometrics 6: 241-252.). The species were classified as to substrate colonized, based on Robbins (1952)ROBBINS RG. 1952. Bryophyta Ecology of a dune area in New Zealand. Vegetation. Acta Geobot 4: 1-31. with adaptations, and the absolute frequency of the rare species was classified according to the number of occurrences (> 1 < 5), based on Silva & Pôrto (2007)SILVA MPP & PÔRTO KC. 2007. Composição e riqueza de briófitas epíxilas em fragmentos florestais da Estação Ecológica de Murici, Alagoas. Rev Bras Biociênc 5: 243-245..

RESULTS

Species accumulation curves

Less than 25% of the species were shared between the five areas, which include four taxa of mosses - Calymperes erosum Müll. Hal., Calymperes palisotii Schwägr., Microcalpe subsimplex (Hedw.) W.R. Buck, and Octoblepharum albidum Hedw. - and three of liverworts - Cheilolejeunea comans (Spruce) R.M.Schust., Cheilolejeunea oncophylla (Aongström) Grolle & E.Reiner, and Cheilolejeunea rigidula (Mont.) R.M.Schust.

Rare species represented about 63% (26) of the sample; 11 species were represented by one occurrence each and five species by two occurrences each. The presence of these levels of rarity contributed to the non-stabilization of accumulation curves, as demonstrated by the fact that there was no saturation of species in the five sampled areas and seasons (Figure 1a-d).

Figure 1
Species accumulation curves in the sampled Park Savanna areas and seasons, Marajó Island, Pará. (a) all areas per dry season; (b) all areas per rainy season; (c) all areas; (d) all areas per rainy and dry season.

Floristic composition

Three hundred and sixteen samples of bryophytes were analyzed, resulting in 41 species with 820 occurrences. Liverworts had a higher richness, with Lejeuneaceae (24 spp., 306 occurrences) followed by Frullaniaceae (two spp., four occurrences). Mosses (15 spp.) were more abundant, with 510 occurrences, of which 383 belonged to Calymperaceae (five spp.), especially Calymperes palisotii Schwägr. (108) and Octoblepharum albidum Hedw. (206), which were widely distributed in the studied areas (Table II). There was a predominance of acrocarpous over pleurocarpous mosses, with 78% (11) of the species distributed in the families Bryaceae, Calymperaceae, Fissidentaceae, Leucobryaceae, and Orthotrichaceae.

Table II
List of bryophytes of the five Park Savanna areas in Marajó Island, Pará.

Species composition

The species composition of SP-V differed significantly from other areas (Pseudo-F = 4.111; p-value = 0.0001) (Figure 2a), and there were five indicator species: Acrolejeunea emergens (Mitt.) Steph., Acrolejeunea torulosa (Lehm & Lindenb.) Schiffn., Microlejeunea epiphylla Bischl., Fissidens guianensis Mont., and Frullania exilis Taylor. SP-I was significantly different only from SP-II and SP-III (p-value = 0.0234; p-value = 0.0069), with Campylopus surinamensis Müll. Hal. and Cheilolejeunea trifaria (Reinw. et al.) Mizut. as indicator species. The sets of SP-I and SP-IV presented similar bryoflora in both seasons, as observed in the large overlap of these groups (Figure 2a).

Figure 2
Principal Component Analysis of bryophytes of the Marajó Island, Pará. (a) Sampled savanna áreas; (b) Seasons.

No significant variation was observed in species composition between wet and dry season (Pseudo-F = 1.7059; p-value = 0.1081) due to the large overlap of groups (Figure 2b). The first two dimensions of the PCA explained 59.8% of the variance in the data set; the first dimension accounted for 39.7%, and the second for 20.1%.

Density, richness and diversity

SP-V presented a significantly different density (Kruskal-Wallis = 23,176; p-value = 0.0001168) (Figure 3a) and richness (Kruskal-Wallis = 22,914; p-value = 0.0001317) in relation to the other sampled areas (Figure 3b).

Figure 3
Mean density and richness of species per plot in the studied areas and seasons in Marajó island, Pará. (a) Mean density in the five Park Savanna areas; (b) Mean richness in the five Park Savanna areas; (c) Mean density in the two seasons; (d) Mean richness in the two seasons.

Seasonality did not influence the density of bryophytes (W = 515; p-value = 0.3393) (Figure 3c), but richness was significantly lower in the dry season (t = 2.0939; p-value = 0.04065) (Figure 3d). The number of species in the dry season was about 86% of the species recorded during the rainy season (31 against 36). Most species (26 spp.) occurred in both seasons and less than one quarter was exclusive of the dry (five spp.) or rainy (10 spp.) season.

The interaction plots indicated that there were variations in the number of occurrences and species among the savannas in the rainy and dry season, but seasonality did not significantly affect the mean density (Figure 4a) and richness (Figure 5b). The diagrams showed that the area was the main factor influencing the density (Figure 4b and c) and richness (Figure 5b and c) of bryophytes in the savannas sampled, with SP-V standing out among the others.

Figure 4
(a) Mean density of bryophytes in the sampled savannas per season; (b) Interaction plot between sampled areas and seasons on mean density of bryophytes; (c) Interaction plot between seasons and sampled areas on mean density of bryophytes.
Figure 5
(a) Mean richness of bryophytes in the sampled savannas per season; (b) Interaction plot between sampled areas and seasons on mean richness of bryophytes; (c) Interaction plot between seasons and sampled areas on mean richness of bryophytes.

Fisher’s alpha indices were consistent with changes in species richness and abundance ​​between sampled areas and seasons, with a pattern of increasing diversity, richness and abundance indices, as well as with species accumulation curves, with higher values ​​for SP-V (8.80) in both seasons (Table III).

Table III
Fisher’s alpha values calculated for the bryophyte community.

Ecological groups

More than half of the species were generalist (30 spp.), found throughout the height of host trees. They were followed by the sun specialists (11 spp.). There was a significant variation in the density of generalist species between the sampled areas (Kruskal-Wallis = 30.54; p-value = 0.0005) (Figure 6a), with significant difference between areas I and II (p-value = 0.001) and III (p-value = 0.006), between areas II and V (p-value = 0.005), between areas III and V (p-value = 0.005), and between areas IV and V (p-value = 0.0008). The richness of the generalist species also varied between the sampled areas (Kruskal-Wallis = 25.019; p-value = 0.0005) (Figure 6b), with significant differences between area I and II (p-value = 0.001) and III (p-value = 0.009), between areas II and V (p-value < 0.005), and between areas IV and V (p-value = 0.005).

Figure 6
Generalist species in the sampled areas. (a) Density; (b) Richness.

Distribution of bryophytes by substrate

The corticolous species were predominant with 88.7% (728) of occurrences, observed along the host trees. Dead trunks were the second most colonized substrates, with 8.4% (69) of occurrences of the epyxilic species, followed by termite mounds (1.9%, 16) and soil (0.8%, seven).

Rare species (26 spp.) were mostly established in live substrates, of which 84% (22) were in live substrate samples, and of these, 17 species occurred on SP-V and with low values ​​in SP-I and SP-IV (six spp.), SP-II (three spp.) and SP-III (one sp.). Of the 32 species recorded in SP-V, 29 (270 occurrences) were found on live trunks and 16 on dead branches; only the taxa Microlejeunea bullata (Taylor) Steph. and Trichosteleum papillosum (Hornsch.) A. Jaeger occurred exclusively on dead branches, while the others occurred synchronously in the two substrates.

DISCUSSION

Accumulation curves

The non-stabilization of accumulation curves in floristic studies in tropical forests is common due to the overrepresentation of rare species. In the case of bryophytes in the Amazon, the predominance of rare species has been cited for the Caxiuanã National Forest in Pará, in non-flooded areas and floodplains, “campinas”, “campinaranas”, and savanna vegetation (Alvarenga & Lisboa 2009ALVARENGA LDP & LISBOA RCL. 2009. Contribuição para o conhecimento da taxonomia, ecologia e fitogeografia de Briófitas da Amazônia Oriental. Acta Amaz 39: 495-504.). Schilling & Batista (2008)SCHILLING AC & BATISTA JLF. 2008. Curva de acumulação de espécies e suficiência amostral em florestas tropicais. Rev Bras Bot 31: 179-187. pointed out that the widespread distribution of rare species is common in tropical forests and contributes to an marked growing trend in species accumulation curves.

Highly represented rare species in certain sites, such as in the savannas studied, are considered by Myers et al. (2000)MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GAB & KENT J. 2000. Biodiversity hotspots for conservation priorities. Nat 403: 853-858. to represent a group with great importance to the conservation of biological diversity.

Species composition

The results indicated that the composition was influenced by local conditions of the habitat rather than by seasonality. Since, although all areas were classified as Park Savanna, differences were observed in terms of density of host trees and soil drainage influenced by riverine forests. Rainfall occurs throughout the year in the Amazon, but two rain periods can be distinguished: one rainiest season influenced by the Intertropical Convergence Zone (ITCZ), and another dry season, with undefined dry season (Fisch et al. 1998FISCH G, MARENGO JA & NOBRE CA. 1998. Uma Revisão Geral Sobre O Clima da Amazônia. Acta Amaz 28: 101-126.). In this sense, the results were expected that the composition would not be influenced by seasonality, considering that most bryophytes are perennial with life cycles with more than one year (necessary for a reproductive cycle and ripening of the spores) and therefore live both wet and dry seasons several times (Geissler 1982GEISSLER P. 1982. Alpine Communities. In: Smith AJE (Ed), Bryophyte Ecology. Springer: Dordrecht, p. 167-189.). On the other hand, a minority of bryophytes are ephemeral with very short life cycles that probably vary with seasonality, such as the moss model Physcomitrium (Cove et al. 2006COVE D, BEZANILLA M, HARRIES P & QUATRANO R. 2006. Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57: 497-520.).

SP-V presented 11 exclusive species, nine of which occurred in live trunks and two in dead trunks. These results indicate that the amount of host trees, light incidence, and the structural and chemical conditions of the substrates are vital for the creation of different microhabitats (Hylander 2009HYLANDER K. 2009. No increase in colonization rate of boreal bryophytes close to propagule sources. Ecol 90: 160-169., Sundberg 2013SUNDBERG S. 2013. Spore rain in relation to regional sources and beyond. Ecography 36: 364-373., Lonnell et al. 2014LONNELL N, JONSSON BG & HYLANDER K. 2014. Production of diaspores at the landscape level regulates local colonisation: an experiment with a spore-dispersed moss. Ecography 37: 591-598.). These conditions act as environmental filters that influence the composition of the bryoflora (Raabe et al. 2010RAABE S, MÜLLER J, MANTHEY M, DÜRHAMMER O, TEUBER U, GÖTTLEIN A, FÖRSTER B, BRANDL R & BÄSSLER C. 2010. Drivers of bryophyte diversity allow implications for forest management with a focus on climate change. For Ecol Manage 260: 1956-1964.) and shape plant communities (Mota-de-Oliveira & ter Steege 2015MOTA-DE-OLIVEIRA S & TER STEEGE H. 2015. Bryophyte communities in the Amazon forest are regulated by height on the host tree and site elevation. J Ecol 103: 441-450.).

The predominance of Lejeuneaceae in the sampled savannas is explained by the fact that this family comprises about 70% of Amazonian bryophyte richness, due to its wide morphological plasticity that allows the colonization of different environments and height zones in host trees (Gradstein et al. 2001GRADSTEIN SR, CHURCHILL SP & 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., Oliveira & ter Steege 2013OLIVEIRA SM & 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 2018MOTA-DE-OLIVEIRA S. 2018. The double role of pigmentation and convolute leaves in Community assemblage of Amazonian epiphytic Lejeuneaceae. PeerJ 6: 1-15.). However, in spite of the greater richness of Lejeuneaceae, the number of occurrences recorded in the sampled savannas was not as high as that of Calymperaceae and Sematophyllaceae. Similar results were found by Bôas-Bastos & Bastos (1998)BÔAS-BASTOS SBV & BASTOS CJP. 1998. Briófitas de uma área de Cerrado no município de Alagoinhas, Bahia, Brasil. Trop Bryol 15: 101-110. in a savanna in Bahia, where Frullaniaceae and Lejeuneaceae were the only liverwort families present. Such families have great ecological amplitude and are common in xerophytic vegetation, although they are usually represented by few occurrences. These families were also the most represented among liverworts recorded in savannas of the Federal District (Câmara & Leite 2005CÂMARA PE & LEITE RN. 2005. Bryophytes from Jalapão, state of Tocantins, northern Brazil. Trop Bryol 26: 23-29.), Goiás (Pinheiro et al. 2012PINHEIRO EMA, FARIA ALA & CÂMARA PEAS. 2012. Riqueza de espécies e diversidade de Marchantiophyta (hepáticas) de Capões de Mata, no Parque Nacional da Chapada dos Veadeiros, Goiás, Brasil. Rev Biol Neotrop 9: 19-27., Aquino et al. 2015AQUINO HF, RESENDE ILM, PERALTA DF & ROCHA LM. 2015. Bryoflora of Gallery Forest in Quirinópolis, Goiás State, Brazil. Hoehnea 42: 419-424., Rios et al. 2016RIOS ABM, OLIVEIRA JPS, SILVA RP, OLIVEIRA-NETO JF, OLIVEIRA LS, PERALTA DF & MACCAGNAN DHB. 2016. Bryophyte diversity in an area of Brazilian Cerrado in Central-West. Neotrop Biol Conserv 11: 132-140.) and Maranhão (Oliveira et al. 2018OLIVEIRA RR, MEDEIROS DL, OLIVEIRA HC & CONCEIÇÃO GM. 2018. Briófitas de área sob o domínio fitogeográfico do Cerrado e novas ocorrências para o Maranhão e região Nordeste do Brasil. Iheringia, Sér Bot 73: 191-195., Costa et al. 2018COSTA AMR, OLIVEIRA RR, SÁ NAS & CONCEIÇÃO GM. 2018. Briófitas do Cerrado Maranhense, Nordeste do Brasil. Rev NBC 8: 33-45.).

The predominance of acrocarpous moss families is common in open, sunny, dry, xeric or anthropic habitats (Bastos & Bôas-Bastos 2008BASTOS CJP & BÔAS-BASTOS SBV. 2008. Musgos acrocárpicos e cladocárpicos (Bryophyta) da reserva ecológica da Michelin, Igrapiúna, Bahia, Brasil. Sitientibus, Sér Ciên Biol 8: 275-279., Širka et al. 2019ŠIRKA P, GALVÁNEK D, TURISOVÁ I & SABOVLJEVIĆ M. 2019. What are the main drivers affecting the pattern of bryophyte life history traits at two contrasting spoil heaps? Flora 253: 17-26.) because these taxa are more resistant to dehydration (Govindapyari et al. 2012GOVINDAPYARI H, KUMARI P, BAHUGUNA YM & UNIYAL PL. 2012. Evaluation of species richness of acrocarpous mosses in Imphal District, Manipur, India. Taiwania 57: 14-26.). For example, turf life form, leaves imbricate and slightly folded, smaller leaves, lengthy costa, leaves with papilla, leaves with hairpoint and hyalocysts/hyaline cells, confers desiccation resistance the acrocarpous mosses and are the result of xerophytic adaptations (Watson 1914WATSON W. 1914. Xerophytic Adaptations of Bryophytes in Relation to Habitat. Physiologist 8: 149-190., Frahm 2003FRAHM JP. 2003. Manual of tropical Bryology. Trop Bryol 23: 1-196., Kürschner 2004KÜRSCHNER H. 2004. Life strategies and adaptations in bryophytes from the nearand Middle east. Turkish J Bot 28: 73-84., Kürschner & Parolly 2005KÜRSCHNER H & PAROLLY G. 2005. Ecosociological studies in Ecuadorian bryophyte communities III. Life forms, life strategies and ecomorphology of the submontane and montane epiphytic vegetation of S Ecuador. Nova Hedwigia 80: 89-113., Henriques et al. 2017HENRIQUES DSG, AH-PENG C & GABRIEL R. 2017. Structure and applications of BRYOTRAIT-AZO, a trait database for Azorean bryophytes. Cryptogam Bryol 38: 137-152.). Similar results were recorded in savanna of Minas Gerais, where acrocarpous mosses accounted for roughly 53% of moss species (Sousa & Câmara 2015SOUSA RV & CÂMARA PEAS. 2015. Survey of the bryophytes of a gallery forest in the National Park of Serra do Cipó, Minas Gerais, Brazil. Acta Bot Bras 29: 24-29.). The moss families recorded in this study were also found in savannas of the Central Plateau (Câmara & Leite 2005CÂMARA PE & LEITE RN. 2005. Bryophytes from Jalapão, state of Tocantins, northern Brazil. Trop Bryol 26: 23-29., Câmara et al. 2005CÂMARA PEAS, OLIVEIRA JRPM & SANTIAGO MMM. 2005. A checklist of the bryophytes of Distrito Federal (Brasília, Brazil). Trop Bryol 26: 133-140., Peralta et al. 2008PERALTA DF, BORDIN J & YANO O. 2008. New mosses records (Bryophyta) for Goiás and Tocantins states, Brazil. Acta Bot Bras 22: 834-844., Sousa et al. 2010SOUSA MAR, GOMES-KLEIN VL & YANO O. 2010. Musgos (Bryophyta) do Parque Estadual da Serra dos Pireneus, Goiás, Brasil. Rev Biol Neotrop 7: 7-26., Porfírio-Júnior et al. 2016PORFÍRIO-JÚNIOR ED, ARAÚJO WS & GOMES-KLEIN VL. 2016. Efeito da cobertura de palmeiras e da distância da floresta sobre a distribuição de musgos na Floresta Nacional de Silvânia, Goiás, Brasil. Rev Biol Neotrop 13: 1-7.).

Calymperaceae and Sematophyllaceae particularly prominent families as colonizers of disturbed or dry environments in the Amazon, represented mainly by Calymperes palisotii Schwägr., Microcalpe subsimplex (Hedw.) W.R. Buck and Octoblepharum albidum Hedw. (Bastos & Yano 1993BASTOS CJP & YANO O. 1993. Musgos da zona urbana de Salvador, Bahia. Hoehnea 20: 21-31., Lisboa & Ilkiu-Borges 1995LISBOA RCL & ILKIU-BORGES AL. 1995. Diversidade das Briófitas de Belém (PA) e seu potencial como indicadoras de poluição. Bol Mus Para Emílio Goeldi 11: 199-225., Visnadi & Monteiro 1990VISNADI SR & MONTEIRO R. 1990. Briófitas da cidade de Rio Claro, Estado de São Paulo, Brasil. Hoehnea 17: 71-84.). The peculiar physiological characteristics of these groups confers them specialized desiccation tolerance mechanisms (Wagner et al. 2014WAGNER S, BADER MY & ZOTZ G. 2014. Physiological Ecology of Tropical Bryophytes. In: Hanson DT & Rice SK (Eds), Photosynthesis in Bryophytes and Early Land Plants. New York: Springer, p. 269-290.).

The greater abundance of mosses than liverworts in dry sites may be related to more members of this lineage having specialized morphological, anatomical, and physiological traits of desiccation tolerance (Proctor & Tuba 2002PROCTOR MCF & TUBA Z. 2002. Poikilohydry and Homeohydry: Antitheses or spectrum of possibilities? New Phytologist 156: 327-349., Proctor et al. 2007PROCTOR MCF, OLIVER MJ, WOOD AJ, ALPERT P, STARK LR, CLEAVITT NL & MISHLER BD. 2007. Desiccation-tolerance in bryophytes: a review. Bryologist 110(4): 595-621., Goffinet et al. 2009GOFFINET B, BUCK WR & SHAW AJ. 2009. Morphology, anatomy, and classification of the Bryophyta. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge: Cambridge, p. 55-138.), which can survive successfully in deserts or extreme environments, especially at high temperatures (Mertens et al. 2008MERTENS J, BELADJAL L, ALCANTARA A, FOUGNIES L, STRAETEN DVD & CLEGG JS. 2008. Sobrevivência de eucariotos secos (anidrobiotes) após exposição a temperaturas muito altas. Rev Biol Soc Linn 93: 15-22.). As for example, dry mosses can survive at exposed temperatures of habitats above 70-110 ºC (Lange 1955LANGE OL. 1955. Untersuchungen über die Hitzeresistenz der Moose in Beziehung zu ihrer Verbreitung. I. Die Resistenz stark ausgetrockneter Moose. Flora Allg Bot Zeit 142: 381-399.), some up to 85-110 ºC, while moist mosses are damaged or do not survive at temperatures of 42-51 ºC (Nörr 1974NÖRR M. 1974. Hitzeresistenz bei Moosen. [Heat resistance of mosses.]. Flora 163: 388-397.). Among the morphological traits associated with desiccation tolerance in mosses, stand out the coast of leaves that aid in rapid absorption and transport of water, in addition to structural support to leaves during desiccation (Frahm 1985FRAHM JP. 1985. A Bryophyte in an Ant Garden. Bryol Times 34(1).); hyaline cells at the base of the leaves that store water to prevent desiccation (Frahm 2003FRAHM JP. 2003. Manual of tropical Bryology. Trop Bryol 23: 1-196.) and turf life forms and acrocarpous habit, which decreases water loss by evaporation and reduces radiation damage to photosynthetic cells, optimizes water absorption rain or air humidity (Vitt 1979VITT DH. 1979. The moss flora of the Auckland Islands, New Zealand, with a consideration of habitats, origins, and adaptations. Can J Bot 57(20): 2226-2263., Kürschner 2004KÜRSCHNER H. 2004. Life strategies and adaptations in bryophytes from the nearand Middle east. Turkish J Bot 28: 73-84.).

Among the most frequent taxa that were shared among the savannas and seasons, Calymperes palisotii Schwägr., Microcalpe subsimplex (Hedw.) W.R. Buck and Octoblepharum albidum Hedw. stood out; they have hyaline cells that accumulate water to prevent desiccation and protect photosynthetic cells from sun damage (Kürschner 2004KÜRSCHNER H. 2004. Life strategies and adaptations in bryophytes from the nearand Middle east. Turkish J Bot 28: 73-84.). The greater occurrence of Calymperes erosum Müll. Hal. in the rainy season (35 against 15) is in line with the ecological descriptions made by Lisboa (1993)LISBOA RCL. 1993. Musgos Acrocárpicos do Estado de Rondônia. Mus Para Emílio Goeldi, Coleção Adolpho Ducke, 272 p., who portrayed this species as widely distributed in humid places such as riverine forests or also in more open areas such as savannas. Thus, C. erosum has become an important model to understand the dynamics of Amazonian savannas, since its greater occurrence has been associated to the recovery of degraded areas (Lopes et al. 2016LOPES MO, PIETROBOM MR, CARMO DM & PERALTA DF. 2016. Estudo comparativo de comunidades de briófitas sujeitas a diferentes graus de inundação no município de São Domingos do Capim, PA, Brasil. Hoehnea 43: 159-171.).

Among liverworts, the species Acrolejeunea torulosa (Lehm. & Lindenb.) Schiffn., Cheilolejeunea oncophylla (Aongström) Grolle & E.Reiner, Cheilolejeunea rigidula (Nees ex Mont.) R.M. Schust. and Microlejeunea epiphylla Bischl. are cited for the Amazon as having morphological traits influenced by the microclimatic conditions of the different height zones of host trees (Mota-de-Oliveira 2018MOTA-DE-OLIVEIRA S. 2018. The double role of pigmentation and convolute leaves in Community assemblage of Amazonian epiphytic Lejeuneaceae. PeerJ 6: 1-15.), with asexual propagules, convoluted leaves and cell wall thickening observed more frequently in the canopy, where irradiance is more intense.

Density, richness and diversity

The low values ​​of density and richness of the savannas sampled in comparison to other tropical ecosystems may be related to their microclimatic conditions such as intense light incidence and low water availability. These conditions act as environmental filters determining the number and mutual species that can coexist, implying the sharing of resources (Slack 1990SLACK NG. 1990. Bryophytes and ecological niche theory. Bot J Linnean Soc 104: 187-213.) and prevent the coexistence of species in long-term equilibrium (Werner 1979WERNER P. 1979. Competition and coexistence of similar species. In: Solbrig OT, Jain S, Johnson GB & Raven PH (Eds), Topics in Plant Population Biology. Columbia University Press, p. 287-310.). Thus, only the most tolerant species are able to establish in the climatic conditions of this environment (Bello et al. 2010BELLO F ET AL. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiver Conserv 19: 2873-2893., Smith & Stark 2014SMITH RJ & STARK LR. 2014. Habitat vs. dispersal constraints on bryophyte diversity in the Mojave Desert, USA. J Arid Environ 102: 76-81.). The variations in density and richness patterns observed in the communities of SP-V in relation to the other areas may be associated with a greater amount of resources present in the environment (Corrales et al. 2010CORRALES A, DUQUE A, URIBE J & LONDOÑO J. 2010. Abundance and diversity patterns of terrestrial bryophyte species in secondary and planted montane forests in the northern portion of the Central Cordillera of Colombia. Bryologist 113: 8-21.) and high variability of microhabitats with favorable conditions for colonization, respectively (Holz et al. 2002HOLZ I, GRADSTEIN SR, HEINRICHS J & KAPPELLE M. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105: 334-348.).

Most mosses and liverworts species are perennial, some exceptions such as Archidium globiferum and Riccia are annual, respectively (Frahm 1996FRAHM JP. 1996. Diversity, life strategies, origins and distribution of tropical inserlberg bryophytes. An Inst Biol/Bot 67(1): 73-86.). In this sense, the greatest exclusive occurrence of species recorded during the rainy season of this study can be explained by the passage of fire in the dry season that often affects vegetation, where extreme ecological conditions reduce the species number of bryophyte (Frahm 1996FRAHM JP. 1996. Diversity, life strategies, origins and distribution of tropical inserlberg bryophytes. An Inst Biol/Bot 67(1): 73-86.), in addition, fire is a factor that reduces the chances of developing a diversified bryoflora (Inácio-Silva et al. 2017INÁCIO-SILVA M, CARMO DM & PERALTA DF. 2017. As espécies brasileiras endêmicas de Campylopus Brid. (Bryophyta) estão ameaçadas? Uma análise usando modelagem para avaliar os seus estados de conservação. Hoehnea 44(3): 464-472.).

In this study, the richness of bryophyte communities followed the same pattern of other Amazonian lowland ecosystems, in which the specific richness of liverworts is always greater than that of mosses (Richard 1984, Brito & Ilkiu-Borges 2013BRITO ES & ILKIU-BORGES AL. 2013. Bryoflora of the municipalities of Soure and Cachoeira do Arari, on Marajó Island, in the state of Pará, Brazil. Acta Bot Bras 27: 124-141., Garcia et al. 2014GARCIA ET, ILKIU-BORGES AL & TAVARES-MARTINS ACC. 2014. Brioflora de duas florestas de terra firme na Área de Proteção Ambiental do Lago de Tucuruí, PA, Brasil. Hoehnea 41: 499-514., Pantoja et al. 2015PANTOJA ACC, ILKIU-BORGES AL, TAVARES-MARTINS ACC & GARCIA ET. 2015. Bryophytes in fragments of Terra Firme forest on the great curve of the Xingu River, Pará state, Brazil. Braz J Biol 75: 238-249., Fagundes et al. 2016FAGUNDES DN, TAVARES-MARTINS AC, ILKIU-BORGES AL, MORAES ER & SANTOS RCP. 2016. Riqueza e aspectos ecológicos das comunidades de briófitas (Bryophyta e Marchantiophyta) de um fragmento de Floresta de Terra Firme no Parque Ecológico de Gunma, Pará, Brasil. Iheringia, Sér Bot 71: 72-84.). On the other hand, the pattern of number of occurrences found was similar to that recorded in dry forests, as is the case of savannas of the Central Plateau, where mosses are better represented in terms of richness and occurrences than liverworts (Bôas- Bastos & Bastos 1998, Visnadi 2004VISNADI SR. 2004. Distribuição da brioflora em diferentes fisionomias de cerrado da Reserva Biológica e Estação Experimental de Mogi-Guaçu, SP, Brasil. Acta Bot Bras 18: 965-973., Câmara et al. 2005CÂMARA PEAS, OLIVEIRA JRPM & SANTIAGO MMM. 2005. A checklist of the bryophytes of Distrito Federal (Brasília, Brazil). Trop Bryol 26: 133-140., Aquino et al. 2015AQUINO HF, RESENDE ILM, PERALTA DF & ROCHA LM. 2015. Bryoflora of Gallery Forest in Quirinópolis, Goiás State, Brazil. Hoehnea 42: 419-424., Rios et al. 2016RIOS ABM, OLIVEIRA JPS, SILVA RP, OLIVEIRA-NETO JF, OLIVEIRA LS, PERALTA DF & MACCAGNAN DHB. 2016. Bryophyte diversity in an area of Brazilian Cerrado in Central-West. Neotrop Biol Conserv 11: 132-140., Costa et al. 2018COSTA AMR, OLIVEIRA RR, SÁ NAS & CONCEIÇÃO GM. 2018. Briófitas do Cerrado Maranhense, Nordeste do Brasil. Rev NBC 8: 33-45., Oliveira et al. 2018OLIVEIRA RR, MEDEIROS DL, OLIVEIRA HC & CONCEIÇÃO GM. 2018. Briófitas de área sob o domínio fitogeográfico do Cerrado e novas ocorrências para o Maranhão e região Nordeste do Brasil. Iheringia, Sér Bot 73: 191-195.).

The low diversity of bryophytes recorded in the studied savannas may be related to the microclimatic conditions, which result from the interaction between substrate quality, pH, temperature, light and humidity (Weibull & Rydi 2005). Among the intrinsic conditions of this vegetation, the prevalent prolonged droughts and lack of nutrients hinder the succession of new species that are not adapted to this ecosystem (Franco 2005FRANCO AC. 2005. Biodiversidade de forma e função: implicações ecofisiológicas das estratégias de utilização de água e luz em plantas lenhosas do Cerrado. In: Scariot A, Sousa-Silva JC & Felfili JM (Eds), Cerrado: Ecologia, Biodiversidade e Conservação. Ministério do Meio Ambiente: Brasília-DF, p. 179-196.). As observed by Bastos & Bôas-Bastos (2008)BASTOS CJP & BÔAS-BASTOS SBV. 2008. Musgos acrocárpicos e cladocárpicos (Bryophyta) da reserva ecológica da Michelin, Igrapiúna, Bahia, Brasil. Sitientibus, Sér Ciên Biol 8: 275-279., the diversity of bryophytes is affected by the regime of fires, as well as by the low availability of water in savannas, for they affect the reproduction and development of these plants. On the other hand, Holz et al. (2002)HOLZ I, GRADSTEIN SR, HEINRICHS J & KAPPELLE M. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105: 334-348. pointed out that the high diversity of bryophytes found in dense forests occurs due to the great diversification of microhabitats that are distributed from the base to the canopy of trees, as well as in rotting trunks and soil.

Ecological groups

The greater abundance of the generalist species is associated with areas under environmental disturbance (Pantoja et al. 2015PANTOJA ACC, ILKIU-BORGES AL, TAVARES-MARTINS ACC & GARCIA ET. 2015. Bryophytes in fragments of Terra Firme forest on the great curve of the Xingu River, Pará state, Brazil. Braz J Biol 75: 238-249., Fagundes et al. 2016FAGUNDES DN, TAVARES-MARTINS AC, ILKIU-BORGES AL, MORAES ER & SANTOS RCP. 2016. Riqueza e aspectos ecológicos das comunidades de briófitas (Bryophyta e Marchantiophyta) de um fragmento de Floresta de Terra Firme no Parque Ecológico de Gunma, Pará, Brasil. Iheringia, Sér Bot 71: 72-84.) or areas that are typically open (like savannas). Generalist species possess great ecological amplitude and greater desiccation tolerance (Lopes et al. 2016LOPES MO, PIETROBOM MR, CARMO DM & PERALTA DF. 2016. Estudo comparativo de comunidades de briófitas sujeitas a diferentes graus de inundação no município de São Domingos do Capim, PA, Brasil. Hoehnea 43: 159-171.). The widespread occurrence of generalist species in the sampled areas demonstrates their tolerance to xerophytic environments, colonizing several substrate types and occurring near forest edges and in more open areas with high light levels (Cerqueira et al. 2015CERQUEIRA GR, ILKIU-BORGES AL, MANZATTO AG & MACIEL S. 2015. Briófitas de um fragmento de floresta ombrófila aberta no município de Porto Velho e novas ocorrências para Rondônia, Brasil. Biota Amaz 5: 71-75.). Brito & Ilkiu-Borges (2013)BRITO ES & ILKIU-BORGES AL. 2013. Bryoflora of the municipalities of Soure and Cachoeira do Arari, on Marajó Island, in the state of Pará, Brazil. Acta Bot Bras 27: 124-141. reported seven generalist species for the savannas of the municipality of Soure, namely, Calymperes palisotii Schwägr., Cheilolejeunea oncophylla (Aongström) Grolle & E.Reiner, Cheilolejeunea rigidula (Nees ex Mont.) R.M. Schust. and Lejeunea laetevirens Nees & Mont. These generalist species are also found in the present study. Other species, including Microcalpe subsimplex (Hedw.) W.R. Buck and Octoblepharum albidum Hedw., are cited by Brito & Ilkiu-Borges (2014)BRITO ES & ILKIU-BORGES AL. 2014. Briófitas de uma área de Terra Firme no município de Mirinzal e novas ocorrências para o estado do Maranhão, Brasil. Iheringia, Sér Bot 69: 133-142. as the best adapted taxa for growth and establishment in a variety of environmental conditions.

The absence of canopy in the savannas and increased availability of light (Ribeiro & Walter 2008RIBEIRO JF & WALTER BMT. 2008. As Principais Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP & Ribeiro JF (Eds), Cerrado: Ecologia e Flora. Brasília-DF: Embrapa, 406 p.) allowed the sun specialists to be found along different gradients, from the base to the top of the trees and shrubs, because light levels and desiccation tolerance are linked and crucial factors that influence the distribution of bryophytes (Király et al. 2013KIRÁLY I, NASCIMBENE J, TINYA F & ODOR P. 2013. Factors influencing epiphytic bryophyte and lichen species richness at different spatial scales in managed temperate forests. Biodiv Conserv 22: 209-223.). Shade specialists were also rarely found near the treetops, because they are more common in moist and shaded forests (Gradstein et al. 2001GRADSTEIN SR, CHURCHILL SP & 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.). According to Wagner et al. (2014)WAGNER S, BADER MY & ZOTZ G. 2014. Physiological Ecology of Tropical Bryophytes. In: Hanson DT & Rice SK (Eds), Photosynthesis in Bryophytes and Early Land Plants. New York: Springer, p. 269-290., species with lower desiccation tolerance do not resist the high light incidence and water stress, and they are therefore mostly excluded from the environment.

Distribution of bryophytes in the substrates

The highest incidence of corticolous species in this study (88%) is also predominant in non-flooded forests in the Amazon (Saldanha et al. 2018SALDANHA LS, PINTO MN, ALMEIDA R, SANTOS VS & LIMA RA. 2018. Caracterização morfológica de briófitas no Município de Benjamin Constant-AM. Biota Amaz 8: 48-52., Oliveira-da-Silva & Ilkiu-Borges 2018OLIVEIRA-DA-SILVA FR & ILKIU-BORGES AL. 2018. Briófitas (Bryophyta e Marchantiophyta) das cangas da Serra dos Carajás, Pará, Brasil. Rodriguésia 69: 1405-1416.) and savannas of the Central Plateau (Aquino et al. 2015AQUINO HF, RESENDE ILM, PERALTA DF & ROCHA LM. 2015. Bryoflora of Gallery Forest in Quirinópolis, Goiás State, Brazil. Hoehnea 42: 419-424.). Decomposing trunks are the following most colonized substrate (Richards 1984RICHARDS 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.). The greater availability of live trunks and increased pH and water retention capacity of barks (Studlar 1982STUDLAR SM. 1982. Host specificity of epiphytic bryophytes near mountain lake Virginia. Bryologist 85: 37-50., Richards 1984RICHARDS 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., Hallingbäck & Hodgetts 2000HALLINGBÄCK T & HODGETTS N. 2000. Mosses, Liverworts, and Hornworts. Status Survey and Conservation Action Plan for Bryophytes. IUCN/SSC Bryophyte Specialist Group. IUCN, Gland, Switzerland and Cambridge, 106 p.) are favorable conditions for the colonization of bryophytes with limited desiccation tolerance mechanisms (Proctor & Tuba 2002PROCTOR MCF & TUBA Z. 2002. Poikilohydry and Homeohydry: Antitheses or spectrum of possibilities? New Phytologist 156: 327-349., Proctor 2008PROCTOR MCF. 2008. Physiological ecology. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Cambridge Press, Cambridge, p. 237-267., Oliveira-da-Silva & Ilkiu-Borges 2018OLIVEIRA-DA-SILVA FR & ILKIU-BORGES AL. 2018. Briófitas (Bryophyta e Marchantiophyta) das cangas da Serra dos Carajás, Pará, Brasil. Rodriguésia 69: 1405-1416.). It is believed that host trees available in savannas are the refuge of bryophytes which seek greater availability of water, where bryophytes are often observed in humid microhabitats such as cracks in tree trunks. Thus, to ensure the maintenance of the communities of bryophytes it is essential that there be the conservation of the plant community, since the richness of species of bryophytes and vascular plants is positively correlated (Ingerpuu et al. 2001INGERPUU N, VELLAK K, KUKK T & PÄRTEL M. 2001. Bryophyte and vascular plant species richness in boreo-nemoral moist forests and mires. Biodivers Conserv 10: 2153-2166.).

The abundance of corticolous species observed in this study is distinct from the pattern found in dense tropical forests with high levels of precipitation. In these forests, substrate preference is neutralized by high humidity; most species have weak or no preference for substrate types, and are able to colonize a variety of available environments (Frahm 2003FRAHM JP. 2003. Manual of tropical Bryology. Trop Bryol 23: 1-196.). Germano & Pôrto (2006)GERMANO SR & PÔRTO KC. 2006. Bryophyte communities in Atlantic forest remnant, state of Pernambuco, Brazil. Cryptogam Bryol 27: 153-163. pointed out that 87% of the bryophytes of a remnant area of ​​the Atlantic Forest with high annual precipitation (2,450 mm) did not show strong preferences for specific substrates.

The exclusive occurrence of Fissidens prionodes Mont. in soil and the low representation of terrestrial species (1.95%) may be related to the variety of morphological traits of this genus, such as presence of limbidium and papillae that act in desiccation tolerance (Pursell 2007PURSELL RA. 2007. Fissidentaceae. Flora Neotrop 101: 1-278., Bordin & Yano 2013BORDIN J & YANO O. 2013. Fissidentaceae (Bryophyta) do Brasil. Bol Inst Bot 22: 1-72.). The chemical composition of the soil of savannas, particularly the acidity, high saturation of aluminum, poor drainage, and low fertility, may be a hindering factor for the colonization of species other, less specialized (Cavalcante et al. 2014CAVALCANTE CO, FLORES AS & BARBOSA RI. 2014. Fatores edáficos determinando a ocorrência de leguminosas herbáceas em savanas amazônicas. Acta Amaz 44: 379-386.). These conditions reinforce the general idea that soil acidification may be responsible for the decline of bryophyte richness (Delgado & Ederra 2013DELGADO V & EDERRA A. 2013. Long-term changes (1982–2010) in the biodiversity of Spanish beech forests assessed by means of Ellenberg indicator values of temperature, nitrogen, light and pH. Biol Conserv 157: 99-107.). Müller et al. (2019)MÜLLER J, BOCHC S, PRATIC D, SOCHERC AS, POMMERA U, HESSENMÖLLERE D, SCHALLI P, SCHULZEE ED & FISCHERC M. 2019. Effects of forest management on bryophyte species richness in Central European forests. For Ecol Manage 432: 850-859. observed that the richness of terrestrial bryophytes decreased with decreasing soil pH in managed forests of Central Europe. Moreover, the abundant grass layer mainly represented by Poaceae and Cyperaceae in the sampled savannas (Bastos 1984BASTOS MNC. 1984. Levantamento florístico dos campos do Estado do Pará. I - Campo de Joanes (Ilha de Marajó). Bol Mus Para Goeldi 1: 67-86.) may be a limiting factor for terrestrial bryophytes, as observed by Jagodziński et al. (2015)JAGODZIŃSKI AM, DYDERSKI MK, GDULA AK, RAWLIK M & KASPROWICZ M. 2015. Zróżnicowanie flory roślin naczyniowych runa pod drzewostanami powstałymi w wyniku rekultywacji zwałowiska pokopalnianego. Stud. Mater. CEPL W Rogowie 42: 249-261., who reported that grasses competed with bryophytes in the soil.

CONCLUSION

This study reveals that bryophytes in savannas of the Marajó Island are well adapted to the environmental conditions of this ecosystem, indicated by the high representation of the generalists and sun specialists among the species, with specialized desiccation tolerance strategies. It was observed that despite the greater availability of water in the rainy season, there is no sufficient succession of new species to prove the influence of this abiotic variable on the structure of the bryophyte communities. In this context, these results were expected, since most bryophytes are perennials, whose life cycle is longer than one year and would be found in both wet and dry seasons. In turn, differences between the sampled areas were the main factor explaining the changes in the composition, richness, density, and diversity of bryophytes.

The sampled savannas presented a richness of bryophytes similar to the other Amazonian ecosystems and the number of occurrences had the same pattern of representation of savannas from the Central Plateau, where mosses are more abundant despite lower levels of species richness than liverworts. Finally, the high frequency of rare species endorses the need for conservation of this ecosystem.

REFERENCES

  • ALVARENGA LDP & LISBOA RCL. 2009. Contribuição para o conhecimento da taxonomia, ecologia e fitogeografia de Briófitas da Amazônia Oriental. Acta Amaz 39: 495-504.
  • AQUINO HF, RESENDE ILM, PERALTA DF & ROCHA LM. 2015. Bryoflora of Gallery Forest in Quirinópolis, Goiás State, Brazil. Hoehnea 42: 419-424.
  • AYRES M, AYRES-ÚNIOR M, AYRES DL & SANTOS AA. 2007. BIOESTAT - Aplicações estatísticas nas áreas das Ciências Bio-Médicas. Belém: Mamirauá, 364 p.
  • BASTOS CJP & BÔAS-BASTOS SBV. 2008. Musgos acrocárpicos e cladocárpicos (Bryophyta) da reserva ecológica da Michelin, Igrapiúna, Bahia, Brasil. Sitientibus, Sér Ciên Biol 8: 275-279.
  • BASTOS CJP & YANO O. 1993. Musgos da zona urbana de Salvador, Bahia. Hoehnea 20: 21-31.
  • BASTOS MNC. 1984. Levantamento florístico dos campos do Estado do Pará. I - Campo de Joanes (Ilha de Marajó). Bol Mus Para Goeldi 1: 67-86.
  • BELLO F ET AL. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiver Conserv 19: 2873-2893.
  • BÔAS-BASTOS SBV & BASTOS CJP. 1998. Briófitas de uma área de Cerrado no município de Alagoinhas, Bahia, Brasil. Trop Bryol 15: 101-110.
  • BORDIN J & YANO O. 2013. Fissidentaceae (Bryophyta) do Brasil. Bol Inst Bot 22: 1-72.
  • BRITO ES & ILKIU-BORGES AL. 2013. Bryoflora of the municipalities of Soure and Cachoeira do Arari, on Marajó Island, in the state of Pará, Brazil. Acta Bot Bras 27: 124-141.
  • BRITO ES & ILKIU-BORGES AL. 2014. Briófitas de uma área de Terra Firme no município de Mirinzal e novas ocorrências para o estado do Maranhão, Brasil. Iheringia, Sér Bot 69: 133-142.
  • BUCK WR. 2003. Guide to the Plants of Central French Guiana. Part 3. Mosses. (Memoirs of the New York Botanical Garden 76). The New York Bot Gar Press, New York.
  • CÂMARA PE & LEITE RN. 2005. Bryophytes from Jalapão, state of Tocantins, northern Brazil. Trop Bryol 26: 23-29.
  • CÂMARA PEAS, OLIVEIRA JRPM & SANTIAGO MMM. 2005. A checklist of the bryophytes of Distrito Federal (Brasília, Brazil). Trop Bryol 26: 133-140.
  • CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahhs. Nat Ecol Evol 1: 1-3.
  • CAVALCANTE CO, FLORES AS & BARBOSA RI. 2014. Fatores edáficos determinando a ocorrência de leguminosas herbáceas em savanas amazônicas. Acta Amaz 44: 379-386.
  • CERQUEIRA GR, ILKIU-BORGES AL, MANZATTO AG & MACIEL S. 2015. Briófitas de um fragmento de floresta ombrófila aberta no município de Porto Velho e novas ocorrências para Rondônia, Brasil. Biota Amaz 5: 71-75.
  • CORRALES A, DUQUE A, URIBE J & LONDOÑO J. 2010. Abundance and diversity patterns of terrestrial bryophyte species in secondary and planted montane forests in the northern portion of the Central Cordillera of Colombia. Bryologist 113: 8-21.
  • COSTA AMR, OLIVEIRA RR, SÁ NAS & CONCEIÇÃO GM. 2018. Briófitas do Cerrado Maranhense, Nordeste do Brasil. Rev NBC 8: 33-45.
  • COSTA DP & PERALTA DF. 2015. Bryophytes diversity in Brazil. Rodriguésia 66(4): 1-9.
  • COVE D, BEZANILLA M, HARRIES P & QUATRANO R. 2006. Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57: 497-520.
  • CRANDALL-STOTLER B, STOTLER RE & LONG DG. 2009. Morphology and classification of the Marchantiophyta. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge, Cambridge, p. 1-54.
  • DELGADO V & EDERRA A. 2013. Long-term changes (1982–2010) in the biodiversity of Spanish beech forests assessed by means of Ellenberg indicator values of temperature, nitrogen, light and pH. Biol Conserv 157: 99-107.
  • DORREPAAL E, AERTS R, CORNELISSEN JHC, CALLAGHAN TV & VAN LOGTESTIJN RSP. 2004. Summer warming and increased winter snow cover affect Sphagnum fuscum growth, structure and production in a sub-arctic bog. Glob Change Biol 10: 93-104.
  • DUFRÊNE M & LEGENDRE P. 1997. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecol 67: 345-366.
  • DUNN OJ. 1964. Multiple comparisons using rank sums. Technometrics 6: 241-252.
  • ELMENDORF SC ET AL. 2012. Global assessment ofexperimental climate warming on tundra vegetation: heterogeneity overspace and time. Ecol Lett 15: 164-175.
  • FAGUNDES DN, TAVARES-MARTINS AC, ILKIU-BORGES AL, MORAES ER & SANTOS RCP. 2016. Riqueza e aspectos ecológicos das comunidades de briófitas (Bryophyta e Marchantiophyta) de um fragmento de Floresta de Terra Firme no Parque Ecológico de Gunma, Pará, Brasil. Iheringia, Sér Bot 71: 72-84.
  • FEARNSIDE PM. 2015. Pesquisa sobre conservação na Amazônia brasileira e a sua contribuição para a manutenção da biodiversidade e uso sustentável das florestas tropicais. In: Vieira I, Jardim M & Rocha E. Amazônia em Tempo: Estudos Climáticos e Socioambientais. Universidade Federal do Pará, Museu Paraense Emílio Goeldi and Embrapa Amazônia Oriental, Belém, p. 21-49.
  • FISCH G, MARENGO JA & NOBRE CA. 1998. Uma Revisão Geral Sobre O Clima da Amazônia. Acta Amaz 28: 101-126.
  • FLORSCHÜTZ-DE WAARD J. 1996. Sematophyllaceae. Musci III. In: Görts-Van Rijn ARA (Ed), Flora of the Guianas. Series C: Bryophytes Fascicle 1: 439-462.
  • FRAHM JP. 1985. A Bryophyte in an Ant Garden. Bryol Times 34(1).
  • FRAHM JP. 1996. Diversity, life strategies, origins and distribution of tropical inserlberg bryophytes. An Inst Biol/Bot 67(1): 73-86.
  • FRAHM JP. 2003. Manual of tropical Bryology. Trop Bryol 23: 1-196.
  • FRANCO AC. 2005. Biodiversidade de forma e função: implicações ecofisiológicas das estratégias de utilização de água e luz em plantas lenhosas do Cerrado. In: Scariot A, Sousa-Silva JC & Felfili JM (Eds), Cerrado: Ecologia, Biodiversidade e Conservação. Ministério do Meio Ambiente: Brasília-DF, p. 179-196.
  • GARCIA ET, ILKIU-BORGES AL & TAVARES-MARTINS ACC. 2014. Brioflora de duas florestas de terra firme na Área de Proteção Ambiental do Lago de Tucuruí, PA, Brasil. Hoehnea 41: 499-514.
  • GEISSLER P. 1982. Alpine Communities. In: Smith AJE (Ed), Bryophyte Ecology. Springer: Dordrecht, p. 167-189.
  • GERMANO SR & PÔRTO KC. 2006. Bryophyte communities in Atlantic forest remnant, state of Pernambuco, Brazil. Cryptogam Bryol 27: 153-163.
  • GLIME JM. 2017. Field Taxonomy and Collection Methods. Chapt. 1. In: Glime JM (Ed), Bryophyte Ecology. V. 3. Methods. Ebook Michigan Technological University and the International Association of Bryologists, 20 p.
  • GOFFINET B, BUCK WR & SHAW AJ. 2009. Morphology, anatomy, and classification of the Bryophyta. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Press Cambridge: Cambridge, p. 55-138.
  • GOSSELIN M, FOURCIN D, DUMAS Y, GOSSELIN F, KORBOULEWSKY N, TOÏGO M & VALLET P. 2017. Influence of forest tree species composition on bryophytic diversity in mixed and pure pine (Pinus sylvestris L.) and oak (Quercus petraea (Matt.) Liebl.) stands. For Ecol Manage 406: 318-329.
  • GOVINDAPYARI H, KUMARI P, BAHUGUNA YM & UNIYAL PL. 2012. Evaluation of species richness of acrocarpous mosses in Imphal District, Manipur, India. Taiwania 57: 14-26.
  • GRADSTEIN SR, CHURCHILL SP & 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 & 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.
  • HALLINGBÄCK T & HODGETTS N. 2000. Mosses, Liverworts, and Hornworts. Status Survey and Conservation Action Plan for Bryophytes. IUCN/SSC Bryophyte Specialist Group. IUCN, Gland, Switzerland and Cambridge, 106 p.
  • HE X, HEB KS & HYVÖNEN J. 2016. Will bryophytes survive in a warming world? PERSPECT Plant Ecol 19: 49-60.
  • HENRIQUES DSG, AH-PENG C & GABRIEL R. 2017. Structure and applications of BRYOTRAIT-AZO, a trait database for Azorean bryophytes. Cryptogam Bryol 38: 137-152.
  • HESPANHOL H, SÉNECAA A, FIGUEIRA R & SÉRGIO C. 2011. Microhabitat effects on bryophyte species richness and community distribution on exposed rock outcrops in Portugal. Plant Ecol Divers 4: 251-264.
  • HOFFMANN WA, JACONIS S, MCKINLEY K, GEIGER E, GOTSH S & FRANCO AC. 2012. Fuels or microclimate? Understanding the drivers of fire feedbacks at savannah forest boundaries. Aust Ecol 37: 634-643.
  • HOLZ I, GRADSTEIN SR, HEINRICHS J & KAPPELLE M. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105: 334-348.
  • HSIEH TC, MA KH & CHAO A. 2013. iNEXT online: interpolation and extrapolation (Version 1.0) [Software]. Available in: http://chao.stat.nthu.edu.tw/blog/software-download/
    » http://chao.stat.nthu.edu.tw/blog/software-download/
  • HYLANDER K. 2009. No increase in colonization rate of boreal bryophytes close to propagule sources. Ecol 90: 160-169.
  • IBGE. 2012. Manual Técnico da Vegetação Brasileira. 2nd ed., Rio de Janeiro: Departamento de Recursos Naturais e Estudos Ambientais, 271 p.
  • INÁCIO-SILVA M, CARMO DM & PERALTA DF. 2017. As espécies brasileiras endêmicas de Campylopus Brid. (Bryophyta) estão ameaçadas? Uma análise usando modelagem para avaliar os seus estados de conservação. Hoehnea 44(3): 464-472.
  • INGERPUU N, VELLAK K, KUKK T & PÄRTEL M. 2001. Bryophyte and vascular plant species richness in boreo-nemoral moist forests and mires. Biodivers Conserv 10: 2153-2166.
  • JAGODZIŃSKI AM, DYDERSKI MK, GDULA AK, RAWLIK M & KASPROWICZ M. 2015. Zróżnicowanie flory roślin naczyniowych runa pod drzewostanami powstałymi w wyniku rekultywacji zwałowiska pokopalnianego. Stud. Mater. CEPL W Rogowie 42: 249-261.
  • KIRÁLY I, NASCIMBENE J, TINYA F & ODOR P. 2013. Factors influencing epiphytic bryophyte and lichen species richness at different spatial scales in managed temperate forests. Biodiv Conserv 22: 209-223.
  • KÜRSCHNER H. 2004. Life strategies and adaptations in bryophytes from the nearand Middle east. Turkish J Bot 28: 73-84.
  • KÜRSCHNER H & PAROLLY G. 2005. Ecosociological studies in Ecuadorian bryophyte communities III. Life forms, life strategies and ecomorphology of the submontane and montane epiphytic vegetation of S Ecuador. Nova Hedwigia 80: 89-113.
  • LANG SI, CORNELISSEN JHC, HOELZER A, TER BRAAK CJF, AHRENS M, CALLAGHAN TV & AERTS R. 2009. Determinants of cryptogam composition and diversity inSphagnum-dominated peatlands: the importance of temporal, spatial andfunctional scales. J Ecol 97: 299-310.
  • LANGE OL. 1955. Untersuchungen über die Hitzeresistenz der Moose in Beziehung zu ihrer Verbreitung. I. Die Resistenz stark ausgetrockneter Moose. Flora Allg Bot Zeit 142: 381-399.
  • LISBOA RCL. 1993. Musgos Acrocárpicos do Estado de Rondônia. Mus Para Emílio Goeldi, Coleção Adolpho Ducke, 272 p.
  • LISBOA RCL & ILKIU-BORGES AL. 1995. Diversidade das Briófitas de Belém (PA) e seu potencial como indicadoras de poluição. Bol Mus Para Emílio Goeldi 11: 199-225.
  • LONNELL N, JONSSON BG & HYLANDER K. 2014. Production of diaspores at the landscape level regulates local colonisation: an experiment with a spore-dispersed moss. Ecography 37: 591-598.
  • LOPES MO, PIETROBOM MR, CARMO DM & PERALTA DF. 2016. Estudo comparativo de comunidades de briófitas sujeitas a diferentes graus de inundação no município de São Domingos do Capim, PA, Brasil. Hoehnea 43: 159-171.
  • MAGURRAN AE. 1988. Ecological diversity and its measurement. New Jersey: Princeton University Press, Princeton.
  • MERTENS J, BELADJAL L, ALCANTARA A, FOUGNIES L, STRAETEN DVD & CLEGG JS. 2008. Sobrevivência de eucariotos secos (anidrobiotes) após exposição a temperaturas muito altas. Rev Biol Soc Linn 93: 15-22.
  • MOTA-DE-OLIVEIRA S. 2018. The double role of pigmentation and convolute leaves in Community assemblage of Amazonian epiphytic Lejeuneaceae. PeerJ 6: 1-15.
  • MOTA-DE-OLIVEIRA S & TER STEEGE H. 2015. Bryophyte communities in the Amazon forest are regulated by height on the host tree and site elevation. J Ecol 103: 441-450.
  • MÜLLER J, BOCHC S, PRATIC D, SOCHERC AS, POMMERA U, HESSENMÖLLERE D, SCHALLI P, SCHULZEE ED & FISCHERC M. 2019. Effects of forest management on bryophyte species richness in Central European forests. For Ecol Manage 432: 850-859.
  • MUSTIN K ET AL. 2017. Biodiversity, threats and conservation challenges in the Cerrado of Amapá, an Amazonian savana. Nat Conserv 22: 107-127.
  • MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GAB & KENT J. 2000. Biodiversity hotspots for conservation priorities. Nat 403: 853-858.
  • NÖRR M. 1974. Hitzeresistenz bei Moosen. [Heat resistance of mosses.]. Flora 163: 388-397.
  • OKSANEN J, KINDT R, LEGENDRE P, O’HARA B, HENRY M & STEVENS H. 2007. Vegan: Community Ecology Package. R package, version 1.8-8. 2007. Available in: http://cran.r-project.org/, http://r-forge.r-project.org/ projects/vegan/
    » http://cran.r-project.org/, http://r-forge.r-project.org/ projects/vegan/
  • OLIVEIRA-DA-SILVA FR & ILKIU-BORGES AL. 2018. Briófitas (Bryophyta e Marchantiophyta) das cangas da Serra dos Carajás, Pará, Brasil. Rodriguésia 69: 1405-1416.
  • OLIVEIRA RR, MEDEIROS DL, OLIVEIRA HC & CONCEIÇÃO GM. 2018. Briófitas de área sob o domínio fitogeográfico do Cerrado e novas ocorrências para o Maranhão e região Nordeste do Brasil. Iheringia, Sér Bot 73: 191-195.
  • OLIVEIRA SM & TER STEEGE H. 2013. Floristic overview of the epiphytic bryophytes of terra firme forests across the Amazon basin. Acta Bot Bras 27: 347-363.
  • PANTOJA ACC, ILKIU-BORGES AL, TAVARES-MARTINS ACC & GARCIA ET. 2015. Bryophytes in fragments of Terra Firme forest on the great curve of the Xingu River, Pará state, Brazil. Braz J Biol 75: 238-249.
  • PARDOW A & LAKATOS M. 2013. Desiccation tolerance and global change: implications for tropical bryophytes in lowland forests. Biotropica 45: 27-36.
  • PERALTA DF, BORDIN J & YANO O. 2008. New mosses records (Bryophyta) for Goiás and Tocantins states, Brazil. Acta Bot Bras 22: 834-844.
  • PINHEIRO EMA, FARIA ALA & CÂMARA PEAS. 2012. Riqueza de espécies e diversidade de Marchantiophyta (hepáticas) de Capões de Mata, no Parque Nacional da Chapada dos Veadeiros, Goiás, Brasil. Rev Biol Neotrop 9: 19-27.
  • PLOTKIN RL & RIDING S. 2011. Biogeography of the Llanos de Moxos: natural and anthropogenic determinants. Biogeogr Llanos Moxos 66: 183-192.
  • PORFÍRIO-JÚNIOR ED, ARAÚJO WS & GOMES-KLEIN VL. 2016. Efeito da cobertura de palmeiras e da distância da floresta sobre a distribuição de musgos na Floresta Nacional de Silvânia, Goiás, Brasil. Rev Biol Neotrop 13: 1-7.
  • PRANCE GT. 1996. Islands in Amazonia. Philos Trans Royal Soc/London 351: 823-833.
  • PROCTOR MCF. 2008. Physiological ecology. In: Goffinet B & Shaw AJ (Eds), Bryophyte Biology, 2nd ed., University Cambridge Press, Cambridge, p. 237-267.
  • PROCTOR MCF, OLIVER MJ, WOOD AJ, ALPERT P, STARK LR, CLEAVITT NL & MISHLER BD. 2007. Desiccation-tolerance in bryophytes: a review. Bryologist 110(4): 595-621.
  • PROCTOR MCF & TUBA Z. 2002. Poikilohydry and Homeohydry: Antitheses or spectrum of possibilities? New Phytologist 156: 327-349.
  • PURSELL RA. 2007. Fissidentaceae. Flora Neotrop 101: 1-278.
  • R CORE TEAM. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: https://cran.r-project.org/bin/windows/base/old/3.1.3/
    » https://cran.r-project.org/bin/windows/base/old/3.1.3/
  • RAABE S, MÜLLER J, MANTHEY M, DÜRHAMMER O, TEUBER U, GÖTTLEIN A, FÖRSTER B, BRANDL R & BÄSSLER C. 2010. Drivers of bryophyte diversity allow implications for forest management with a focus on climate change. For Ecol Manage 260: 1956-1964.
  • RIBEIRO JF & WALTER BMT. 2008. As Principais Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP & Ribeiro JF (Eds), Cerrado: Ecologia e Flora. Brasília-DF: Embrapa, 406 p.
  • 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.
  • RIOS ABM, OLIVEIRA JPS, SILVA RP, OLIVEIRA-NETO JF, OLIVEIRA LS, PERALTA DF & MACCAGNAN DHB. 2016. Bryophyte diversity in an area of Brazilian Cerrado in Central-West. Neotrop Biol Conserv 11: 132-140.
  • ROBBINS RG. 1952. Bryophyta Ecology of a dune area in New Zealand. Vegetation. Acta Geobot 4: 1-31.
  • ROSSETTI DF, VALERIANO MM & THALLÊS M. 2007. An abandoned estuary within Marajó Insland: implications for late quaternary paleogeography of northern Brazil. Estuar Coasts 30: 813-826.
  • SALDANHA LS, PINTO MN, ALMEIDA R, SANTOS VS & LIMA RA. 2018. Caracterização morfológica de briófitas no Município de Benjamin Constant-AM. Biota Amaz 8: 48-52.
  • SANTOS ND, COSTA DP, KINOSHITA LS & SHEPHERD GJ. 2014. Windborne: Can liverworts be used as indicators of altitudinal gradient in the Brazilian Atlantic Forest? Ecol Indicators 36: 431-440.
  • SCHILLING AC & BATISTA JLF. 2008. Curva de acumulação de espécies e suficiência amostral em florestas tropicais. Rev Bras Bot 31: 179-187.
  • SILVA GFN & OLIVEIRA IJ. 2018. Reconfiguração da paisagem nas savanas da Amazônia. Mercator 17: 1-20.
  • SILVA MPP & PÔRTO KC. 2007. Composição e riqueza de briófitas epíxilas em fragmentos florestais da Estação Ecológica de Murici, Alagoas. Rev Bras Biociênc 5: 243-245.
  • ŠIRKA P, GALVÁNEK D, TURISOVÁ I & SABOVLJEVIĆ M. 2019. What are the main drivers affecting the pattern of bryophyte life history traits at two contrasting spoil heaps? Flora 253: 17-26.
  • SLACK NG. 1990. Bryophytes and ecological niche theory. Bot J Linnean Soc 104: 187-213.
  • SMITH RJ & STARK LR. 2014. Habitat vs. dispersal constraints on bryophyte diversity in the Mojave Desert, USA. J Arid Environ 102: 76-81.
  • SOUSA MAR, GOMES-KLEIN VL & YANO O. 2010. Musgos (Bryophyta) do Parque Estadual da Serra dos Pireneus, Goiás, Brasil. Rev Biol Neotrop 7: 7-26.
  • SOUSA RV & CÂMARA PEAS. 2015. Survey of the bryophytes of a gallery forest in the National Park of Serra do Cipó, Minas Gerais, Brazil. Acta Bot Bras 29: 24-29.
  • STRASSBURG BBN ET AL. 2017. Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1: 0099.
  • STUDLAR SM. 1982. Host specificity of epiphytic bryophytes near mountain lake Virginia. Bryologist 85: 37-50.
  • SUNDBERG S. 2013. Spore rain in relation to regional sources and beyond. Ecography 36: 364-373.
  • VANDERPOORTEN A, PAPP B & GRADSTEIN R. 2010. Sampling of bryophytes. In: Eyman J, Degreef J, Häuser C, Monje, JC, Samyn Y & Vanden-Spiegel D (Eds), Manual on field recording techniques and protocols for All Taxa Biodiversity Inventories and Monitoring. ABC Taxa 8: 340-354.
  • VISNADI SR. 2004. Distribuição da brioflora em diferentes fisionomias de cerrado da Reserva Biológica e Estação Experimental de Mogi-Guaçu, SP, Brasil. Acta Bot Bras 18: 965-973.
  • VISNADI SR & MONTEIRO R. 1990. Briófitas da cidade de Rio Claro, Estado de São Paulo, Brasil. Hoehnea 17: 71-84.
  • VISNADI SR & VITAL DM. 1989. Briófitas rupícolas de um trecho do rio Bethary, Iporanga, estado de São Paulo. Acta Bot Bras 3: 179-183.
  • VITT DH. 1979. The moss flora of the Auckland Islands, New Zealand, with a consideration of habitats, origins, and adaptations. Can J Bot 57(20): 2226-2263.
  • WAGNER S, BADER MY & ZOTZ G. 2014. Physiological Ecology of Tropical Bryophytes. In: Hanson DT & Rice SK (Eds), Photosynthesis in Bryophytes and Early Land Plants. New York: Springer, p. 269-290.
  • WALKER MD ET AL. 2006. Plantcommunity responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103: 1342-1346.
  • WATSON W. 1914. Xerophytic Adaptations of Bryophytes in Relation to Habitat. Physiologist 8: 149-190.
  • WEIBULL H & RYDIN H. 2005. Bryophyte species richness on boulders: Relationship to area, habitat diversity and canopy tree species. Biol Conserv 122: 71-79.
  • WERNER P. 1979. Competition and coexistence of similar species. In: Solbrig OT, Jain S, Johnson GB & Raven PH (Eds), Topics in Plant Population Biology. Columbia University Press, p. 287-310.
  • ZAR JH. 2010. Biostatistical Analysis. 5th ed., Pearson Prentice-Hall, Upper Saddle River, New Jersey.

Publication Dates

  • Publication in this collection
    14 June 2021
  • Date of issue
    2021

History

  • Received
    22 July 2019
  • Accepted
    11 May 2020
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