Diversity of bryophytes in priority areas for conservation in the Atlantic forest of northeast Brazil

The northeastern Brazilian Atlantic forest is the region with the greatest diversity of bryophytes in the country. However, knowledge about bryophytes is irregularly distributed among Brazilian regions. Therefore, we aimed to contribute to knowledge about bryophytes on a regional scale in the northeastern Atlantic forest, to identify the centers of bryophyte diversity in that region, and to reiterate the importance and identify locations for which new protected areas should be created. We built a database of bryophytes in 23 locations of the region, based on a literature review and new floristic inventories. To identify the locations of greatest relevance to bryophyte conservation, we considered 1) total and endemic species richness, 2) phylogenetic diversity (PD), and 3) functional diversity (proportion of shade specialists). The northeastern Atlantic rainforest contains 396 spp., representing 26% of the taxa occurring in the country, 13 of which are endemic. Generalist species predominated (164 spp.), followed by shade (133 spp.) and sun (92 spp.) specialists. The Murici Ecological Station had the highest richness, number of endemic species, and phylogenetic diversity.


Introduction
The Atlantic forest is the phytogeographic domain that shelters the greatest diversity of bryophytes in Brazil (Gradstein et al. 2001).The same authors also state that in the Neotropics, the diversity of bryophytes in the Atlantic Forest is surpassed only by those of the forests of the northern Andes and Central America.In addition, the Atlantic Forest is remarkable for its relevance and urgency of conservation, sheltering 16 of the 17 threatened Brazilian bryophyte species (Fundação Biodiversitas 2005;MMA 2008).
Currently, 378 (94% of all Brazilian) genera and 1,351 (88% of Brazilian) species of bryophytes are recorded for the Atlantic forest (Costa et al. 2014).According to Gradstein & Costa (2003) and Santos et al. (2011), Montane Atlantic Forest areas, particularly in the southeast, have many records of endemic bryophytes, many liverwort species, and interesting affinities with the bryoflora of the Andes.These authors also state that the number of endemic species occurring in the Atlantic coast region is twice that in the Amazon region, including 12 endemic families.With respect to mosses in particular, the endemism level for that domain is even greater with 190 species (20%), whereas only 10 endemic species (1%) are recorded in the Amazon Rainforest (Costa et al. 2011).
Despite its great biodiversity, the Atlantic Forest is one of the main targets of environmental degradation by exploitative human activities, such as the expansion of agriculture and urban areas and logging (Conservação Internacional do Brasil et al. 2000;Angelo 2013).According to Campanili & Prochnow (2006), this is the second most threatened vegetation domain on the planet, the first being the nearly extinct forests of the island of Madagascar off the coast of Africa.In the Brazilian Northeast Atlantic Forest, where the exploitation of forest resources is secular (Tabarelli et al. 2005), large gaps in the knowledge of the distribution of bryophytes in different states are notable.
To the best of our knowledge, this work is the first effort to contribute to the information about bryophytes in the northeastern Atlantic forest on a regional scale and to identify the centers of floristic (total number of species and endemics), phylogenetic (proportions of species and topological differences between them) and functional (proportions of functional groups) diversity for bryophytes.Furthermore, we aimed to test whether these parameters are influenced by a latitude gradient through the northeastern Atlantic forest and to highlight locations where stronger conservation measures, viareinforcement of existing protected areas or creation of new ones, are urgently required.

Study area
The study was conducted in the northern part of the Atlantic Forest, sensu lato, covering the states of Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, and Sergipe (34°51'41"-37º20'32"W, 5º51'00"-10º45'16"S) (Table 1, Fig. 1) (hereafter, northeastern Atlantic forest), covering a linear distance of 595 km from north to south through 6° of latitude.This forest is mainly distributed up to 1,000 m altitude (Tabarelli et al. 2006), including tropical altitudinal wet forests, "Brejo de altitude, " enclaves of moist forest surrounded by a near-desert vegetation (sensu Andrade-Lima 1982).The average temperature in the region is 25 °C and Department of Botany, Federal University of Pernambuco.

Data Analysis
For the determination of endemic taxa of the Atlantic Forest, Gradstein & Costa (2003) and Costa et al. (2011;2014) were consulted.
Phylogenetic diversity (PD) was calculated using an adaptation of the method proposed by Faith (1992).However, for bryophytes, particularly for tropical species, there is no single classification system based on molecular analysis.Thus, the "phylogenetic tree" used was based on the taxonomic hierarchy of species, as indicated by Warwick & Clarke (1995;1998).The calculation was performed with R 2.15.1 using the "vegan" package.
To identify the locations of greatest relevance to the conservation of bryophytes, three criteria were considered: 1) total richness and endemic species of the Atlantic Forest, 2) phylogenetic diversity (PD), and 3) proportion of indicator species for forest conservation (shade specialists).
Simple linear regression was used to identify dependences among these criteria and latitude using Statistica 8.0.Variables were logarithmically transformed (Zar 1999).

Results and discussion
Based on the literature survey, 371 specific taxa were compiled, distributed in 147 genera and 52 families, three  annual precipitation varies between 1,300 and 2,400 mm, with a rainy season from March to September (Veloso et al. 1991).

Database
We built a comprehensive database of the bryophytes of the northeastern Atlantic forest.To this end, we reviewed literature of all bryophyte records in the area to identify sites with systematic bryophyte sampling, resulting in 10 locations that were integrated into the study (Table 1).
After the initial diagnosis of gaps in bryophyte sampling in the Northeast Atlantic Forest, 13 sites were selected to conduct further bryophyte surveys.To identify the highest possible bryoflora diversity, these locations were sampled for three days, during which exploratory walks were taken to collect plant material.Information from this sampling was incorporated into the literature review, so that the total database was composed of 23 sites in the Atlantic rainforest.
Together, the 396 bryophyte species of the northeastern Atlantic forest comprised an appreciable fraction of the total in the country, accounting for 26% of the total diversity of bryophytes in Brazil (1,527 spp.sensu Costa et al. 2014), 10% of the neotropics (4,000 spp.; Gradstein et al. 2001) and 2% of the world (18,000 spp.; Goffinet & Shaw 2009).Furthermore, 101 species were recorded for the first time for at least one of the five Brazilian states sampled.This result shows the importance of broad-scale studies to increase knowledge of Brazilian bryophytes.On the other hand, it also demonstrates sampling gaps in some Brazilian states.For example, Chryso-hypnum diminutivum is a widely distributed species in Brazil, being reported in 20 (77%) Brazilian states (Costa et al. 2014;Silva & Pôrto 2010;2013;Oliveira et al. 2011).However, the present study includes the first record for Paraíba and Sergipe, probably owing to a lack of previous sampling in those areas.This situation can be observed for several other species, such as Fissidens zollingeri and Pilosium chlorophyllum, recorded in 23 (88%) and 24 (92%) of the states of Brazil, respectively (Costa et al. 2014), and here reported for the first time in the state of Rio Grande do Norte.
Certainly owing to the large size of Brazil, studies of bryophyte diversity on a regional scale are rare.The studies of Santos et al. (2011) for the Atlantic Forest and Mota de Oliveira et al. (2009) and Mota de Oliveira ( 2010) for the Amazon rainforest can be cited.Santos et al. (2011) recorded 192 species of bryophytes in Restinga Forest and Lowland Forest areas in the Southeast and found that, when evaluated in terms of landscape, the two forest formations formed distinct floristic groups.However, at the regional level the bryophytes had more affinities with one another than with those of other phyto-physionomically similar areas of the Atlantic Forest.
For the Amazon Rainforest, Mota de Oliveira et al. (2009) and Mota de Oliveira ( 2010) presented a systematic approach to identify community structures of epiphytic bryophytes in a transect from east to west across the Amazon Basin that resulted in the identification of 225 species and 38 morphospecies.For the Atlantic Forest, the present study is the first contribution to the knowledge of communities of bryophytes at the regional level.It was observed that, even considering differences in methodologies, overall bryofloristic richness was higher in the northeastern Atlantic forest than in the Amazon, an observation that is recurrent in the literature (Gradstein et al. 2001;Gradstein & Costa 2003;Costa et al. 2011).In total, 300 species of liverworts (Gradstein & Costa 2003) and 350 species of mosses (Costa et al. 2011) have been registered for the Amazon rainforest, whereas in the Atlantic forest these figures are larger (500 spp. of liverworts and 700 spp. of mosses).However, these authors argue that the great richness of the Atlantic Forest is due to the presence of areas with high elevation (>1000 m), especially in the southeast, which are unusual in the Amazon Rainforest.For the northeast, areas with an altitude between 30 and 990 m were analyzed, and even then, the higher floristic variety of the Atlantic Forest was confirmed.
It is noteworthy that generalist species predominated (164 spp., 41%), followed by specialists in shade (133 spp., 34%) and sun (92 spp., 23%) (for 7 spp., 2%, there was no information on specialism).This result is recurrent in the literature for the Northeast Atlantic Forest (Alvarenga & Pôrto 2007;Silva & Pôrto 2009;2010) and other tropical forests (Acebey et al. 2003).These studies showed that shade specialists are more sensitive to deforestation, and sometimes are completely absent from degraded sites, fol-lowed by sun specialists, whereas generalists are indifferent.Thus, degradation and loss of habitat recurring in the region (sensu Tabarelli et al. 2006) are indicated as causes of the predominance of generalists (Naaf & Wulf 2010).
On the other hand, even though the reserve is still widely covered, most forest fragments do not reach 1,000 ha and all are immersed in a very inhospitable matrix, consisting of pasture for cattle and sugar cane (Silva & Pôrto 2009;Pôrto et al. 2012).Selective logging, firewood, hunting, and animal poaching, particularly of birds for captive breeding and wildlife trafficking (Pôrto et al. 2012), are additional problems.Thus, we emphasize the vital significance of the Conservation Unit for regional bryophytes and suggest the implementation of effective public policies in APA Murici, a buffer zone in areas surrounding the Murici Ecological Station, especially in the areas of remaining private forest belonging to the sugar mills in the region.
It is noteworthy that Fissidens flabellatus and Syrrhopodon brasiliensis, endemic mosses endemic of Brazil, have been reported here for the first time in the Brazilian Northeast, recorded in MET and ITA, respectively.
Despite the high richness and presence of endemic species relevant to conservation in the Northeast Atlantic Forest, logging, cultivation of sugar cane, and hunting are common practices.Thus, we emphasize the vital importance of the Northeast Atlantic Forest to the national bryophytes and suggest the implementation of effective conservation activities in the region, especially in the Murici Ecological Station and FCA as well as in private forest remnants.

Figure 1 .
Figure 1.Location of the Atlantic Forest remnants surveyed in the present study.SeeTable 1 for site names.

Figure 2 .
Figure 2. Representatives of the main families of bryophytes, compiled by literature review and inventory performed in the present study.

Table 1 .
Locations, number of species, and references of the northeastern Atlantic forest sites surveyed in the present study.
Table 1 for site names.

Table 2 .
Phylogenetic diversity (PD), percentage of shade specialist species, and numbers of endemic (Brazilian) species of bryophytes of the northeastern Atlantic forest sites surveyed in the present study.For site abbreviations see Table1.