Bryophyte communities of restingas in Northeastern Brazil and their similarity to those of other restingas in the country

Restingas are a coastal component of the Atlantic Forest. Th ey experience high temperatures and possess soils with a low capacity to retain water, low nutrient content and high salt concentrations. Studies on bryophytes of restingas have been mostly conducted in Southeastern Brazil, and so we aimed to characterize the bryophyte fl ora of seven areas of restinga in the Northeastern Region and to establish their fl oristic affi nities with other restingas in Brazil. Fifty-fi ve species were found in the studied restingas, the vast majority of which are generalist species with life forms of intermediate tolerance to desiccation and of corticicolous and terrestrial habitat. Th e number of species per area is low compared to the species richness of other restingas in Brazil. A cluster analysis, although based on low similarity, showed that the bryofl ora from the surveyed areas is distinct from those of restingas from Bahia, Espírito Santo and Rio de Janeiro, which all form a group, and those of the coast of São Paulo, which also comprised a cluster. Th e heterogeneous climate, soils and vegetation structure of the studied restingas, in comparison those of the Southeast, act as selective fi lters for the species, thereby contributing to the distinction observed in those communities.


Introduction
Brazilian restingas (a type of tropical coastal vegetation) comprise a diverse set of plant communities that extend discontinuously along approximately 80% (7,110 km) of the Atlantic Coast, from 4 °N to 34 °S (Suguio & Tessler 1984).Restingas are recent formations that originated in the Quaternary as result of regressions and transgressions of the sea, with climatic and, mainly, edaphic factors acting as conditioners (Magnago et al. 2013).
Th e vegetation of Brazilian coastal restingas exhibit a wide variety of phytophysiognomies, from open fi elds closer to the sea to forest with canopies of up to 20 meters in height.In these forested areas, organic matter tends to accumulate in the soil and light intensity is lower due to shading by the forest canopy (Scarano 2002;Sampaio et al. 2005).Th e woody fl ora is closely associated with the Atlantic Forest (Pereira 2003).
In general, restinga vegetation withstands limiting conditions because the soils are oligotrophic, salty and have low water retention, plus they experience high temperatures, intense sunlight and strong winds (Rizzini 1997).
Present knowledge regarding the bryophytes of restingas basically comes from areas concentrated in Southeastern Brazil, thanks to the contributions of Behar et al. (1992), Visnadi & Vital (1995) and Silva & Piassi (2010) in the state of Espírito Santo; Costa & Yano (1998), Costa et al. (2006) and Imbassahy et al. (2009) in Rio de Janeiro; and Vital & Visnadi (1994), Yano & Peralta (2004), Visnadi (2010) and Santos et al. (2011) in São Paulo.In contrast, there has been only one study on the bryophytes of restingas of Northeastern Brazil, an inventory by Bastos & Yano (2006) for the metropolitan area of Salvador and the north coast of Bahia.
Thus, the present study represents the first investigation into the bryophytes of the restingas of the coastline between the states of Rio Grande do Norte and Sergipe in Northeastern Brazil.The goal was to determine the floristic composition and characterize the bryophyte communities of these restingas, and to assess their floristic affinities with restingas of Southeastern Brazil.
A standardized sampling effort of five-hours was established in order to explore, by foot, each area as much as possible and to record all vegetation types of each area.Samples were collected from preferred substrates such as live tree trunks (ground level to nearly 2m height), rotting logs and soil.The procedure of collection and herborization of material followed the methodology described by Yano (1989).All voucher material was deposited in the Herbarium UFP Geraldo Mariz of the Federal University of Pernambuco.

Data analysis
Bryophyte floristic composition, species richness (number of species), Shannon diversity index (H') and evenness (J') (Ricklefs 2001) were determined for each area of restinga.
Bryophyte floristic composition was compared among areas by calculating similarities using the Sörensen coefficient and UPGMA (Krebs 1989).Cluster analyses were performed using the software Primer 6.0 (Clarke & Warwick 2001) and adopting values of cophenetic relation of clusters above 0.7 as an indication of satisfactory correspondence (Visnadi & Vital 2001).
In order to assess affinities between the bryofloras of the study areas with those reported for restingas of Bahia and Southeastern Brazil, a matrix of binary data was built by compiling data from the following: Bahia (Bastos & Yano 2006); Espirito Santo (Behar et al. 1992;Visnadi & Vital 1995;Silva & Piassi 2010); Rio de Janeiro (Costa et al. 2006;Imbassahy et al. 2009); and São Paulo (Vital & Visnadi 1994;Yano & Peralta 2004;Visnadi 2010;Santos et al. 2011).This matrix was subjected to the same methodology described for the calculation of floristic similarity.

Results and discussion
The present work provides the first report of bryophyte species composition, richness and similarity for areas of restinga of the coast of Northeastern Brazil.Fifty-five species of bryophytes were recorded (Tab.S1 in supplementary material), among which 27 were mosses and 28 liverworts.

Bryophyte communities of restingas in Northeastern Brazil and their similarity to those of other restingas in the country
Five geographical patterns of distribution were recognized among the bryophytes sampled.Species with a Neotropical distribution (52.7%) predominated, followed by species with Pantropical (31%), Wide (6%) and African-American (5.3%) distributions.One species (5%), Fissidens flabellatus Hornsch, is endemic to Brazil (Bordin & Yano 2013).The sampled species are widely distributed in Brazil, and most have been reported from more than one phytogeographical domain, especially the Atlantic Forest, and none are under threat of extinction (MMA 2008;Martinelli & Moraes 2013).
Generalist species were quantitatively (number of species) and qualitatively (number of samples) more represented, followed by sun tolerant and, finally, shade tolerant species (Tab.1).Most species have a wide range of ecological tolerance, growing in several forest phytophysiognomies as well as open, semi-arid, plantation and urban areas, such as: Acrolejeunea spp., Bryum coronatum, Calymperes afzelli, C. palisotti, Cheilolejeunea rigidula, Lejeunea flava, L. laetevirens, Octoblepharum albidum, Schiffneriolejeunea polycarpa and Sematophyllum spp.(Visnadi & Monteiro 1990;Bastos & Yano 1993;Lisboa & Ilkiu-Borges 1995;Câmara et al. 2003;Yano & Câmara 2004;Bordin & Yano 2009).The pronounced representation of these species is consistent with the environmental characteristics of restingas, wherein intense sunshine, high temperatures and strong winds, among other factors, limit the growth and development of many plant species and dictate the occurrence of those more tolerant.
In turn, life-forms with high (tuft and cushion) or intermediate (mat and carpet) tolerance to desiccation were dominant; the former were found colonizing soil or live trunks, and the latter colonizing live trunks and/or, more rarely, decaying trunks.With respect to sun tolerance, there was greater representation for species with life forms of intermediate desiccation tolerance colonizing live trunks or decayed logs.Shade tolerant species were numerically less abundant and were represented by Fissidens spp., which are tufts and have terrestrial habitat, and by the pendant and corticicolous Squamidium nigricans.Extensive colonization of live trunks and soil undoubtedly reflects the large availability of these types of substrates in the studied environments.Epiphylls were absent, which is not surprising considering the high exposure to solar radiation (Bastos & Yano 2006) and low water retention capacity of leaf surfaces making them an inhospitable substrate for colonization by bryophytes in these environments.
Richness ranged from 12 to 23 species per area, whereas floristic affinity among the seven areas varied between 23 and 66% (Tab.2).Five out of the seven areas inventoried in this study were protected areas, which seems to be a providential action since these areas are close to major urban centers and are highly susceptible to a wide variety of human impacts.It is noteworthy that the restinga with the highest richness of bryophytes in this study (RPPN Nossa Senhora do Outeiro), is located next to an area of intensive tourism, yet is still considered to be of good conservation status (Almeida Jr. et al. 2009).The bryophyte floras of the studied restingas had low species richness in comparison to other Brazilian restingas, and were among the lowest values reported for this type of vegetation (Tab.3).Restingas from Bahia and Southeastern Brazil that were selected for comparative analysis in this study ranged in bryophyte species richness from eight to 175 species.Extensive heterogeneity in bryophyte species richness among restingas has been noted previously, such as for the Parque Nacional da restinga de Jurubatiba, Rio de Janeiro (Imbassahy et al. 2009) and the Parque Estadual Paulo César Vinha in Espírito Santo (Silva & Piassi 2010).The authors of these studies considered ecotonal factors and dissimilarities of vascular communities to be determinants in the differentiation of the non-vascular flora.With regard to the phanerogamic flora, Zickel et al. (2004) also found striking differences in species composition and representativeness between restingas of Southeastern and Northeastern Brazil due to their geomorphological differences.However, more recent work on the vascular flora of restingas of Northeastern Brazil (CS Zickel unpubl.res.) found that geomorphology and abiotic factors were not significant.
Although based on a relatively low degree of similarity (between 22-30%), cluster analysis (cophenetic correlation 0.85) revealed the existence of three groups of restingas based on bryophyte flora: the first is comprised of the restingas of the present study in Northeastern Brazil; the second clusters the restingas from Bahia, Espírito Santo and Rio de Janeiro; and the third group contains exclusively the restingas from São Paulo (Fig. 1).Some species stand out as being reported, to date, only from the Northeastern restingas, although they are common in other vegetation formations, such as Calymperes lonchophyllum, Campylopus gardneri, Fissidens goyazensis, Lejeunea trinitensis and Metalejeunea cucullata.On the other hand, the absence of representatives of Metzgeriaceae, Plagiochilaceae and Radulaceae is remarkable, since they are common in the Southeastern restingas (e.g., Costa et al. 2006;Imbassahy et al. 2009;Visnadi 2010) and relatively widely distributed in remnants of Atlantic Forest in the Northeast.One of factors that may be responsible for limiting the species of these families from occupying the studied restingas may be their more severe limitation of moisture.Restingas of the Southern and Southeastern regions of Brazil have longer periods of soil flooding, which in turn favors increased water content of the soils of these environments due to, mainly, the topography, the depth of the water table, and the proximity of water bodies (Silva 1999).These factors, based on recent studies, influence the distribution of the phanerogamic flora in the restingas of the Southern and Southeastern regions (Assis 2011;Marques et al. 2011).On the other hand, studies that seek to empirically determine what environmental factors affect the spatial distribution of bryophyte species in restingas are absent.Due to their structural and physiological characteristics, bryophytes respond more significantly to microenvironmental than to macroenvironmental variables (e.g.Alvarenga et al. 2010), and so it is reasonable to consider the importance of microenvironmental variables in the distribution of these plants in restingas.
The heterogeneous environmental conditions, geomorphology, soil and vegetation structure and composition of the areas of restinga studied in Northeastern Brazil, compared to those of the Southeast, represent selective filters for the species, and contribute to the observed differences in communities.Moreover, stochastic events, such as dispersion, human interference or other biotic or abiotic variables that were out of the scope of the present study, may be acting on bryophyte composition and must be taken into account in future studies.

Table 1 .
Bryophyte communities of restingas of Northeastern Brazil according to light tolerance, life-form and habitat.Absolute frequencies are provided in parentheses.

Table 3 .
Bryophyte species richness for areas of Brazilian restinga used for comparative analysis in this study.