Open-access Floristic characterization of an Atlantic Rainforest remnant in Southern Sergipe: Crasto forest

Caracterização florística de um remanescente de Mata Atlântica no sul de Sergipe: Mata do Crasto

Abstracts

The state of Sergipe has suffered extreme reduction of its Atlantic Forest area in the last decades. The objective of this study is to present an inventory of the Mata do Crasto flora, the largest Atlantic Forest Remnant in Sergipe (approximately 1,000 ha), located in the Municipality of Santa Luzia do Itanhy. An intensive survey was undertaken with monthly plant collections in the study area, for four years (1995 to 1999). Additionally, collections deposited in herbaria were consulted to complete the species list. A total of 324 species were found, belonging to 84 families and 193 genera. This study adds an additional 29 genera and 96 species to the Sergipe flora as new occurrences. The four most speciose families were the Fabaceae (33 species), Rubiaceae (24 species), Myrtaceae (23 species) and Melastomataceae (15 species), that accounted for ca. 30% of the total species. The taxonomic distinction of the area is very similar to three other lowland forests in Northeastern Brazil, although its species composition is quite distinct.

Flora; Coastal Vegetation; Taxonomic diversity; São Francisco River


O estado de Sergipe sofreu extrema redução da área de Mata Atlântica nas últimas décadas. Este trabalho tem como objetivo inventariar a composição florística da Mata do Crasto, maior remanescente de Mata Atlântica de Sergipe (aproximadamente 1.000 ha), situada no Município de Santa Luzia do Itanhy. Um inventário intensivo foi realizado com coletas florísticas na área de estudo por quatro anos (1995 a 1999). Adicionalmente, exsicatas depositadas em herbários foram consultadas para complementar a lista de espécies. Um total de 324 espécies foram identificadas, pertencentes a 84 famílias e 193 gêneros. Este estudo adicionou 96 espécies è flora de Sergipe como novas ocorrências. As famílias com maior número de espécies são Fabaceae (33 espécies), Rubiaceae (24 espécies), Myrtaceae (23 espécies) e Melastomataceae (15 espécies), que juntas somam cerca de 30% do total de espécies. A distinção taxonômica do remanescente é surpreendentemente similar ao de outras florestas de terras baixas no Nordeste do Brasil embora suas espécies sejam bastante distintas.

Flora; Vegetação costeira; Diversidade taxonômica; Rio São Francisco


Introduction

The Brazilian Atlantic Rainforest is one of the 25 'hotspots' of the world, i.e., areas that have a high concentration of endemic species and that are liable to significant loss of habitat, containing at least 2% of known plants and vertebrates (Myers et al. 2000). Recent surveys of Atlantic Forest recognize 13,708 species and 1,782 genera in 208 families of angiosperms, of which 126 genera (7%) and 6,663 species (49%) are endemic to the forests (Stehmann et al. 2009).

Analyses of the distribution of Atlantic Forest plant species have identified two or more centers of endemism, depending upon the objectives and organisms being considered (Murray-Smith et al. 2008; Fiaschi & Pirani 2009). However, a north-south divide is agreed by most researchers, the northern part of which extends from Rio Grande do Norte to northern Espírito Santo, approximately coinciding with the Rio Doce Valley (Fiaschi & Pirani 2009).

In the northern region of the Atlantic Forest two centers of endemism are recognized: Northern Espírito Santo/Bahia and Pernambuco (Thomas et al. 1998). However, despite the importance and high floristic diversity of the Atlantic Forest (Stehmann et al. 2009), a high percentage of the remaining forest area are still poorly studied and the geographic distribution of many taxa incomplete (Fiaschi & Pirani 2009). Studies of the extant areas are of fundamental importance to establishing hotspots within the Atlantic Forest (Giulietti et al. 2005; Murray-Smith et al. 2008), permitting better understanding of species distributions and understanding the possible effects of the São Francisco River as a geographic barrier.

It has been estimated that only 11.73% of the original Atlantic Forest remains (Ribeiro et al. 2009). The current situation may be a vicious circle; the better studied areas showing a high diversity and therefore concentrating Atlantic Forest conservation investment. In view of the accelerated rhythm of deforestation the Atlantic Forest has experienced to date (Dean 1996), specifically the northern sector (Freyre 2004), it is necessary to ensure that poorly studied areas are inventoried urgently, since many are threatened, in spite of the Brazilian legal protection instruments (Law N° 11.428/2006). Throughout the Atlantic Forest northern sector, the forest fragments are vulnerable, due to their high timber value, and extreme reduction and fragmentation (Ranta et al. 1998; Tabarelli et al. 2006).

In Sergipe, the Atlantic Forest covered the whole coastal zone, occupying a strip approximately 40 km wide. At the beginning of the 20th century, it was estimated that 41% of the state was covered by forests (Campos, 1912); recent estimates show that Atlantic Forest covers only 9% of its original area in the state (Fundação SOS Mata Atlântica/INPE 2005). In this region, forest vulnerability is increased by the gently rolling landscape and by the low social-economic level of the population which exploits forest fragments for fuelwood, building and hunting.

Sergipe was one of the last Brazilian States to have its flora investigated scientifically. In the 19th century it was visited only by George Gardner, who collected 210 samples from around the mouth of the São Francisco River, in 1838. Although some of these samples state “Bahia” as their location, he goes on to cite the Villa de Propriá (Stephen Harris, OXF, pers. comm.), and Propriá is now part of Sergipe. Herbarium specimens made available by CRIA (2013) reveal only sporadic collections in the 20th century. One collection by J.G. Kuhlmann (RB) from 1923 and some collections by D. Andrade-Lima from the 1950s and 1960s were found. Significant sampling of the Sergipe flora did not start until the 1970s, with the foundation of the ASE herbarium at the Universidade Federal de Sergipe.

The Atlantic Forest fragments of Sergipe have attracted little attention. However, investigations of these fragments have shown they are important for conservation (Landim & Siqueira 2001) because of their floristic diversity, and for harboring rare and threatened animals, such asCallicebus coimbrai, a recently described primate, found almost exclusively in Atlantic Forest remnants of Sergipe (Brasil/MMA 2003, Jerusalinsky et al. 2006, Veiga et al. 2008).

The southern part of Sergipe has several Atlantic Forest remnants important for conservation, and the Litoral e complexo das matas do sul de Sergipe region was considered one of the areas of the highest importance and urgency amongst those selected for immediate action (BRASIL/MMA 2007). The present study aimed to characterize floristically the largest Atlantic Forest fragment in southern Sergipe. Additionally, the flora of this fragment was compared to other fragments in the northern sector of the Brazilian Atlantic Forest, to find similarities between them.

Materials and methods

Study area

This study was undertaken in the Mata do Crasto(11°22' S, 37°25' W), an ombrophilous lowland forest remnant of ca. 1,000 ha, with altitudes from 5 to 90m, located in the Santa Luzia do Itanhy Municipality, Sergipe. The region is situated in the Piauí River basin; its climate is classified as coastal wet with strongly seasonal precipitation, with rainfall concentrated in the middle of the year. Climatic data was obtained from the Meteorological Center of the Secretaria de Estado do Meio Ambiente e dos Recursos Hídricos (SEMARH/SRH). The closest PCD (Plataforma de Coleta de Dados) weather station to the study area, in the city of Estância (ca. 10.5 km from Santa Luzia do Itanhy) registered total rainfall of 794.2 mm and an average temperature of 25.1o C in 2012. Long-term rainfall data from the region, registered an average rainfall of 2,096.2 mm between 1964 and 1985; during this period annual rainfall varied between 1,452.3 and 3,438.5 mm.

Data sampling and analysis

Monthly collections were made in the study area mainly between 1995 and 1999. The material was collected and dried using standard herbarium techniques (Mori et al. 1989) and deposited in the Universidade Federal de Sergipe (ASE) herbarium. Duplicates were distributed to other herbaria, particularly in northeastern Brazil, but also to Universidade de Brasília (UB), Instituto de Botânica de São Paulo (SP), Jardim Botânico do Rio de Janeiro (RB) and Arizona State University (ASU) herbaria.

Family and species circumscription, as well as spelling and authorities adopted for scientific names, followed, except when explicitly informed, the Lista de Espécies da Flora do Brasil (2014). The listed vouchers are those with the widest distribution in herbaria, selected from the examined material. Information on plant habits was obtained from herbarium material and, when these were missing, from the literature. A species was considered as “previously recorded from Sergipe” when it was either cited inLista de Espécies da Flora do Brasil (2014) or in Volume 1 of Flora de Sergipe (Prata et al. 2013).

Taxonomic richness (Warwick & Clarke 1995; Clarke & Warwick 1998) of the Mata do Crastofragment was compared with that of similar floristic inventories (i.e., those that included all angiosperms, independent of habit) and in similar phytophysiognomies (ombrophilous forests or semi-deciduous lowland forests) in other states of the northern sector of the Atlantic Forest. This index, calculated from presence and absence data, records the average distance between two species chosen at random (Clarke & Warwick 1998). The selected inventories had their species lists checked at the data base of the Centro de Referência em Informação Ambiental (http://www.cria.org.br/), in order to identify the existence of more recent determinations, and being afterwards standardized taxonomically, using Lista de Espécies da Flora do Brasil (2014) synonymy or The Plant List (2013).

Vouchers unidentified to species level in original lists were checked against on-line herbaria in Centro de Referência em Informação Ambiental (http://www.cria.org.br/) for possible new determinations. The Taxonomic Distinction Index (Δ+) was calculated using PAST, version 2.14 (Hammer et al. 2001). Four taxonomic levels (order, family, genus and species) were adopted and the same step length (=1) was used to attribute weight to distances between the different levels (Clarke & Warwick 1999).

Results and discussion

Floristic composition

The Mata do Crasto floristic list recorded 324 species of which 21 (6.5%) were identified only to genus and two (0.6%) only to family (Tabel 1). The floristic list recorded 84 families and 193 genera. Over a third of the species were new occurrences for Sergipe: 129 (30%) new species occurrences, 29 new generic occurrences and four new family occurrences (Humiriaceae, Onagraceae, Smilacaceae and Vochysiaceae) according to data available in the Lista de Espécies da Flora do Brasil (2014).

Table 1
List of the 321 species and morphospecies of Angiosperms found in the Atlantic Forest remnant of Mata do Crasto, Santa Luzia do Itanhy, Sergipe, organized in alphabetical order by family with vouchers. * = species absent from the Lista de Espécies da Flora do Brasil (2014).

Although species accepted in the Lista de Espécies da Flora do Brasil (2014) were adopted as the taxonomic standard, three species not recognized by this list (not even as synonyms) were accepted: Trichilia lepidota Mart. subsp.ferruginea T.D. Penn. (Amorim 1484) was maintained since it is an isotype; Tibouchina asperifolia Cogn. (Landim 759) is accepted by The Plant List (2013) and byMelastomataceae.Net (2013); andPisonia cordifolia Mart. ex J.A.Schmidt is an unresolved name in The Plant List (2013) (http://www.theplantlist.org/tpl/record/kew-2552380).

The most speciose families (Figure 1), Fabaceae (33 species), Rubiaceae (24 species), Myrtaceae (23 species) and Melastomataceae (15 species), account for 30% of the species in the Mata do Crasto. These four families are amongst the nine most diverse families in the Atlantic Forest (Stehmann et al. 2009). In a study of Atlantic Forest in southern Bahia, Ubatuba (SP) and Porto Alegre (Rio Grande do Sul) these families were also important but the Fabaceae are more speciose in the Mata do Crasto than in either of these areas and the Myrtaceae, proportionally, less important (Leitão Filho, 1987). However, in a wider and more recent survey of Atlantic Forest, Oliveira-Filho & Fontes’ (2000) conclusions were more similar to those reported here. According to their results, the four most speciose families in the Mata do Crasto are also the five most speciose families in lowland pluvial Atlantic forests, considering the Fabaceae as a single family (sensu APG III, Reveal & Chase 2011). The apparent similarity of theMata do Crasto to other areas should be interpreted with caution since the database used by Oliveira-Filho & Fontes (2000) did not consider areas north of southern Bahia. Differences in collection effort and subtle alterations in methodologies, together with differential attention to forest strata can also influence richness results and bias comparisons of family richness.

Figure 1
. Angiosperm families with five or more species found in theMata do Crasto Atlantic Rainforest remnant, Santa Luzia do Itanhy, Sergipe, Brazil.

In the Mata do Crasto, there are 33 species in 20 genera in the Fabaceae, the second most speciose family in the Atlantic Forest domain (Stehmann et al. 2009), corresponding to 26% and 36%, respectively, of the total numbers of species and genera known in Sergipe (Lima et al. 2013). In surveys of the northeast (Rodal et al. 2005, Barbosa et al., 2011) and in the southeast (Ivanauskas & Rodrigues 2000,Peixoto et al. 2004, Zipparro et al. 2005, Rolim et al. 2006) regions of the Atlantic Forest, the Fabaceae is usually the most speciose family.

The most speciose genera of Fabaceae in the Mata do Crasto wereInga and Senna (four and six species, respectively). Inga is the eighth most speciose genus in lowland pluvial Atlantic forest (Stehmann et al. 2009) and one of the two Fabaceae genera included in the 21 most diverse genera in these communities by Oliveira-Filho & Fontes (2000). Physiognomically,Tachigali densiflora (Benth.) L.F. Gomes da Silva & H.C. Lima, a large emergent tree very characteristic of the Sergipe Atlantic Forest remnants is a prominent component; this Caesalpinoid Legume occurs in Minas Gerais and then northwards in all the coastal states up to northeastern Paraíba (Lima et al. 2013).

The Rubiaceae is the second most speciose family in the Mata do Crasto, with 24 species in 12 genera; 61% and 46% of the total number of Rubiaceae species and genera, respectively, recorded from Sergipe (Barbosa et al. 2013). This family is the ninth most speciose in Atlantic Forest (Stehmann et al. 2009) and the third most speciose in lowland Atlantic pluvial forest (Oliveira-Filho & Fontes 2000). Psychotria andBorreria were the richest genera (seven and four species, respectively).

Seven genera and 23 species of Myrtaceae were recorded from the Mata do Crasto. Although eight genera and 35 species of Myrtaceae are cited from Sergipe in the Lista de Espécies do Brasil (Sobral et al. 2013), recent compilations increase these numbers up to ten genera and 60 species (Proença et al. 2013) . The 23 species of Myrtaceae recorded in this forest remnant correspond to 38% of this latter total.Myrcia (nine species), Eugenia (five species) and Campomanesia (four species) are the most diverse genera. Amongst the genera with most species in lowland pluvial Atlantic forests, Eugenia and Myrcia are two of the most speciose (70 and 37 species, respectively). Marlierea, represented in the Mata do Crasto by a single species,M. excoriata, is the sixth most speciose (22 species; Oliveira-Filho & Fontes 2000).

Myrtaceae is the third most speciose family in the Mata do Crasto, although it was the sixth most speciose family in the Atlantic Forest domain (Stehmann et al. 2009) and the most speciose in lowland pluvial Atlantic Forest (Oliveira-Filho & Fontes 2000). This family appears to be most important in the Southeastern Atlantic forests (Tabarelli & Mantovani 1999, Zipparro et al. 2005, Ivanauskas & Rodrigues, 2000, Peixoto et al. 2004, Rolim et al. 2006).

In the northern sector, Myrtaceae seems to be less important: it was forth most speciose family in a seasonal lowland forest near the coast of Pernambuco (Rodal et al. 2005) and was not even listed amongst the six most speciose families in a survey in coastal Paraíba (Pereira & Alves 2006) or in a study in Alagoas (Oliveira et al. 2005), and it was only seventh in three areas of montane Atlantic forest in southern Bahia (Amorim et al. 2009). However, a survey of an area of lowland Atlantic Forest in Pernambuco (Amorim & Alves 2011) reported the same number of species of Myrtaceae as in this study. Although the distance between the two areas is less than 600 km, these two areas together have 35 species of Myrtaceae, of which 11 were shared.

In a study using Myrcia as an indicator genus of local biodiversity hotspots within the Atlantic Forest domain (Murray-Smith et al. 2008), the Atlantic Forest was subdivided in squares of 1° latitude x 1° longitude, to which nine levels of richness were allocated, based on the number ofMyrcia species present, with level 1 the poorest (“0-1 species”) and level 9 the richest (“29-49 species”). Although the square in which the Mata do Crasto is found (11-12° S x 37-38° W) was classified in their study as level 3 (“5-8 species”), our data, associated with additional collections from the ASE herbarium, have shown that this square actually has at least 13 species of Myrcia and should have been classified in the intermediate level 5 (“12-14 species”). These findings reinforce the relevance of the present study results for the current analyses of the biodiversity distribution pattern in the Brazilian Atlantic Rainforest.

Habits

Most of the species collected in the Mata do Crasto belong to the tree/shrub layer, followed by the subshrub/herb layer. Higher percentages of species in the tree layer were registered in Atlantic Forest fragments in north-eastern and south-eastern Brazil (Table 2), accounting for over half the species in Pernambuco and São Paulo. In a study carried out in another type of forest found in the Brazilian northeast, a fragment of montane forest in the municipality of Brejo da Madre de Deus, in Pernambuco (Nascimento, Rodal & Silva 2012), the tree habit was also the best represented (50% of all species).

Table 2
Comparison between habit distributions of Angiosperm species in the Mata do Crasto, Santa Luzia do Itanhy, Sergipe, and in other Atlantic Forest studies. Values are in percentages. BA = Bahia; PE = Pernambuco; SE = Sergipe; SP = São Paulo.

It was proposed by Gentry & Dodson (1987) that trees contribute relatively little towards the high species diversity in tropical forests, and that is partially confirmed by the significant percentage of lianas, herbaceous climbers and herbs found in this study. Richards (1996) emphasizes the preponderance of woody phanerophytes in tropical rainforests (includes trees as well as shrubs and climbers) and the importance of epiphyte species over ground herbs, stressing, however, the difficulties in comparing life-form spectra from different studies.

A smaller comparative importance of climbers and epiphytes might be expected in the Mata do Crasto, and in forests of the northeast, in general, due to the smaller total rainfall, higher seasonality and high inter-annual variation in precipitation. In fact, the importance of epiphytes in the Mata do Crasto is lower than in almost all other areas with which it was compared in Table 2, suggesting that the quantity and annual distribution of rainfall may limit establishment of epiphytes in this forest fragment. On the other hand, percentages of climbers and lianas are similar to those of forest fragments in Bahia. Although species of epiphytes are sometimes eliminated from the forests with increased disturbance by man, some species may flourish under these conditions (Hietz et al. 2006). Likewise, lianes may be favored by the more open forest canopy that often results from selective cutting and other forms of disturbance (Schnitzer & Bongers 2002).

However, it is possible that the relative importance of non arboreal species may still remain underestimated in many floristic surveys (Linares-Palomino et al. 2009). Although collecting tall trees may be a difficult task, the difficulty in identifying vegetative stage of lianas and epiphytes specimens in the field, and, sometimes, the requirement of specialized equipment to collect them, it is possible that these life forms are yet insufficiently sampled in the Mata do Crasto. Future efforts should concentrate on this layer to strengthen conservation planning that covers the whole diversity of tropical forests, and not only of the tree stratum (Gentry, 1992).

Taxonomic diversity and distinction

Few published floristic studies are comparable to the Mata do Crasto study, encompassing the whole Angiosperm community of a significant remnant of lowland ombrophilous Forest. Most floristic inventories found in Northeastern states include only woody plants and/or were undertaken in different forest types, such as montane, caducifolius and/or inland forests. Only three comparable studies have been found in states of Pernambuco (Rodal et. al 2005) and Alagoas (Oliveira et al. 2005), both north of the São Francisco River, and one in Bahia (Amorim et al. 2008), that is South of the São Francisco River.

A total of 1,457 angiosperm species were recorded across the four sites. The Bahia and Alagoas studies were both the most species-rich and comprehensive, with more than one fragment and several different phytophysiognomies included (Table 3). The Bahia study, undertaken in 9,000 ha of protected area in the REBIO de Una, included adjacent florestas de tabuleiro(restingas litorâneas, a kind of maritime forest). The Alagoas site covered 8,000 ha, including dozens of Atlantic Forest fragments of various sizes and different degrees of human perturbation (Oliveira et al. 2005). Our study in the Mata do Crasto, covering a single fragment of 1,000 ha, ranked third in number of species, while the smallest fragment (81 ha), in Pernambuco (Santos et al. 2001 cited by Rodal et al. 2005), was the one in which the smallest number of species was recorded. The large differences in sampled area amongst three of these studies likely influence the numbers of species recorded. Study area size is strongly correlated with the number of species recorded as large areas are more likely to include different habitats, thereby increasing species richness (Primack & Rodrigues 2001).

Table 3
Angiosperm taxa richness and distribution in selected floristic inventories in lowland Atlantic Forest remnants in Northeastern Brazil. AL = Alagoas; BA = Bahia; PE = Pernambuco; SE = Sergipe.

Little difference in average taxonomic distinction between the four selected lowland Northeastern Atlantic Forest studies was found, values of Δ+ found varying between 3.88 and 3.91 (Table 3). Unfortunately, there are no other Atlantic Forest studies in which measures of taxonomic diversity have been calculated for the complete list of angiosperm species of a region, what may hinder further comparisons. Webbs (2000) study was apparently the first to apply measures of taxonomic diversity and distinctness to angiosperms, analyzing tree species of tropical forests in Borneo. But, with the exception of the work of Dominguez et al. (2010), comparing angiosperm floras in the Hawaiian and Canarian archipelagos, no other study was found encompassing the whole angiosperm flora present in an area.

Measures of diversity that incorporate phylogenetic distance among species are thought to be better than more traditional measures (Cianciaruso, Silva & Batalha 2009). Measures of taxonomic diversity and distinction include a dimension of phylogenetic diversity that is more closely related to functional diversity than species richness. Such indices are apparently less sensitive to sample size than conventional ecological indices, such as richness and equitability. They also appear independent of sampling effort, permitting comparisons among studies with different degrees of sampling effort. However, identification influences all indices and it is critical that care is taken that this is done as completely and as accurately as possible (Clarke & Warwick 1998,1999). Identification is a problem in families where species are notoriously hard to distinguish (e.g., Myrtaceae) and incomplete identification of such families is frequent in floristic studies due to the cryptic nature of distinguishing characters (McVaugh 1968, Landrum and Kawasaki 1997), what did not happen is this study, where all Myrtaceae taxa are identified at species level.

Our values of Δ+ are, however, close to those calculated (3.73 - 3.77) by Gorenstein (2009) for trees in a submontane ombrophilous forest, at altitudes between 30 and 1,003 m, within the Atlantic Forest domain in São Paulo. Lower Δ+ values were found in four Ugandan phytophysiognomies, varying from 2.41, in dry woodland, to 2.79, in dry thicket woodland (Gwali et al. 2010); these data were also based only on the woody flora, using three taxonomic levels (Family, Genus and Species).

The high similarity among the Taxonomic Distinctiness indices between these four areas was unexpected, especially since they differ to each other in total number of families, genera and species, and that all four had many exclusive species (47-75%). Given its intermediate position, both geographically and in size, between the larger (and richer) Bahia and Alagoas sites, the relatively high proportion (51%) of species uniqueness at the Mata do Crasto site is striking. Although physiognomically similar, this data suggests Northeastern Atlantic forests are not floristically uniform.

Usually, large areas have a greater proportion of species per genus and species per family than small areas. In our study, however, the highest proportions of species per family (3.1) were found in Pernambuco, the smallest area; conversely, the number of species per genera (1.3) in this fragment was much lower than elsewhere. Values of species per family for our study (1.6) were between the Alagoas (1.4) and Bahia (1.9) studies; this value thus follows a geographic gradient diminishing northwards. In species per family, however, the Mata do Crasto value (3.6) was lower than either the Bahia (7.3) or Alagoas studies (5.3) that included more than one fragment and forest type.

Shared species between studies was surprisingly low: only 15 species (1%) were common to all four studies, even when possible synonyms were accounted for. Conversely, the number of species exclusive to a single study was very high varying from 85 exclusive species (47%) in Pernambuco to 629 (76%) in Bahia. The Alagoas study and our study showed intermediate values; Alagoas had a higher number of exclusive species (306) than the Mata do Crasto (151), but the percentages of exclusive species were similar (58 and 51%, respectively). Exclusive species thus seem to diminish approximately northwards.

The results were also analyzed considering the São Francisco River (SF) as a potential dispersal barrier. Two hundred and fifteen species (15%) had distributions that crossed the São Francisco river (i.e., that are shared between all, three or two studies that crossed the river). The percentage of exclusive species in the studies south of the São Francisco River (Alagoas and Bahia) is nearly twice (822 species, 56%) that of those North of the river (420 species, 29%); however, these results may be influenced by the different number of fragment and forest types included in these studies (Oliveira, Grillo, & Tabarelli 2005, Amorim et al. 2008). A quantitative association analysis is beyond the scope of this study but it is noteworthy that although Fabaceae was the most speciose family in the three distribution classes (widespread, SF-south, and SP-south), Rubiaceae was the second most important family only amongst the SF-south species (55) and widespread species (19), and was substituted by the Orchidaceae (33 species) in the SF-north species. It was also observed that SF-south species were distributed in more families (114) than either SF-north species (90 families) or widespread species (67 families).

Conclusion

This study has contributed an additional 96 species to the Sergipe flora, and increased knowledge of their geographic distribution and that of other species in the Atlantic forests of the Northeast. Northeastern Atlantic Forest fragments subject to somewhat similar environmental characteristics may have significantly different floristic compositions, and a high proportion of exclusive species, although taxonomic diversity appears to be relatively stable. Considering the strong level of anthropogenic pressure on the northeastern Atlantic Forest remnants, it is possible that much of its native diversity has already been lost, particularly rare species and the ones that are most sensitive to habitat alteration, thus creating false “disjunctions” in their distributions. Other possibilities are that many species have spatial or temporal casuistic mosaic-like distribution patterns, or that the existence of many continuous, but regional, species is responsible for the observed pattern. Additional floristic inventories in Atlantic Forest fragments, particularly, but not exclusively, in the Northeast are needed to clarify individual species' distribution patterns and also forest type distribution patterns.

Studies that increase comprehension of structure, function and environmental causes are necessary to ensure the effective conservation of Atlantic forests. To be effective, these should occur at a rate that preempts the accelerating rates of deforestation. Many threats, and their synergies, lead to a decline in populations of Neotropical tree species, which can produce chains of events that influence ecological services (Tabarelli, Silva & Gascon 2004). Such considerations have lead to some authors questioning the conservation value of small forest fragments for long-term Atlantic Forest preservation (Tabarelli, Mantovani & Peres 1999). In Pernambuco, for example, almost half of the fragments analyzed in the south of the state had an area above 10 ha, but only 7% were above 100 ha (Ranta et al. 1998). This highlights the importance of the Mata do Crasto, an Atlantic Forest fragment of ca. 1,000 ha, for the effective conservation of the floristic and faunistic diversity of the northeastern Atlantic Forest.

Therefore, the first of the recommendations made by Landim & Landrum (2002) regarding the knowledge of Sergipe’s flora, increasing sampling effort, remains valid, but the last two ones must not be forgotten: the urgent need to study Brazil's Northeastern flora, including herbarium material, and a simultaneous investment in taxonomic training. In this context, the first volume of the Flora de Sergipe (Prata et al. 2013) is an important contribution. In order to understand species richness and distribution in Sergipe, other rainforest fragments (in the municipalities of Indiaroba, Itaporanga d’Ajuda, São Cristóvão and Japaratuba) are also being studied and inventoried.

Acknowledgements

This study was partially supported by EMBRAPA-CPATC and CNPq. We are deeply grateful to Eládio dos Santos, ASE herbarium technician, and the former Biology students Adriano Vicente, Andréa Cristina Santos da Cruz, Camila de Santana Amaral and Denise Moura and specialists A.P. Prata, A. Alves-Araujo, A.M. Amorim, A.L. Peixoto, D.C. Daly, J.R. Pirani, L.P. de Queiroz, M.J. da Silva, M.F. de Sales, M.R. Barbosa, M.P.M. de Lima e T.T. Carrijo for kindly identifying material at our request. The “Flora de Sergipe” project financed visits to ASE by botanical specialists that added several welcome new determinations to the species list. We also thank S.A. Harris for reviewing the English version and for information on Gardner's Sergipe collections, and the anonymous reviewers for suggestions made on an earlier draft of the manuscript.

References

  • AMORIM, A.M., JARDIM, J.G., LOPES, M.M.M., FIASCHI, P., BORGES, R.A.X., PERDIZ, R.O. & THOMAS, W.W. 2009. Angiosperms of Montane Forest areas in southern Bahia, Brazil. Biota Neotrop. 9(3): 313-348. http://www.biotaneotropica.org.br/v9n3/en/abstract?inventory+bn02909032009(último acesso em 16/04/2012)., 10.1590/S1676-06032009000300028
    » https://doi.org/10.1590/S1676-06032009000300028» http://www.biotaneotropica.org.br/v9n3/en/abstract?inventory+bn02909032009
  • AMORIM, A.M.A., THOMAS, W.W., CARVALHO, A.M.V. & JARDIM, J.G. 2008. Floristics of the Una Biological Reserve, Bahia, Brazil. The Atlantic Coastal Forests of Northeastern Brazil (WW Thomas, ed.). Mem. New York Bot. Gard. 100: 67-146.
  • AMORIM, B.S. & ALVES, M. 2011. Flora da Usina São José, Igarassu, Pernambuco: Myrtaceae. Rodriguésia, 62(3):499-514.
  • BARBOSA, M.R.V., THOMAS, W.W., ZÁRATE, E.L.P., LIMA, R.B., AGRA, M.F., LIMA, I.B., PESSOA, M.C.R., LOURENÇO, A.R.L., DELGADO JÚNIOR G.C., PONTES, R.A.S., CHAGAS, E.C.O., VIANA, J.L., GADELHA-NETO, P.C., ARAÚJO, C.M.L.R., ARAÚJO, A.A.M., FREITAS, G.B., LIMA, J.R., SILVA, F.O., VIEIRA, L.A.F., PEREIRA, L.A., COSTA, R.M.T., DURÉ, R.C. & SÁ, M.G.V. 2011. Checklist of the vascular plants of the Guaribas Biological Reserve, Paraíba, Brazil. Rev. Nordestina Biol. 20(2):79-106.
  • BARBOSA, M.R., ZAPPI, D., TAYLOR, C., CABRAL, E., JARDIM, J.G., PEREIRA, M.S., CALI=, M.F., PESSOA, M.C.R., SALAS, R., SOUZA, E.B., DI MAIO, F.R., MACIAS, L., ANUNCIAÇÃO, E.A.da & GERMANO FILHO, P.. 2013. Rubiaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/2012/index?tid=210&mode=dp(último acesso em 16/04/2012).
    » http://floradobrasil.jbrj.gov.br/2012/index?tid=210&mode=dp
  • BRASIL/MMA. 2003. Instrução Normativa N° 03, de 27 de maio de 2003. In: Lista Oficial das Espécies da Fauna Brasileira Ameaçadas de Extinção. Ministério do Meio Ambiente (MMA), Brasília. Diário Oficial da União - Seção 1. 101: 88-97.
  • CAMPOS, G. 1912. Mappa Florestal. Ministério da Agricultura, Indústria e Comércio. Secretaria do Estado de Meio Ambiente, São Paulo.
  • CRIA - CENTRO DE REFERÊNCIA EM INFORMAÇÃO AMBIENTAL. Species link. http://www.splink.cria.org.br (último acesso em 16/04/2013).
    » http://www.splink.cria.org.br
  • CLARKE, K.R. & WARWICK, R.M. 1998. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35(4):523-531, 10.1046/j.1365-2664.1998.3540523.x.
    » https://doi.org/10.1046/j.1365-2664.1998.3540523.x
  • CLARKE, K.R. & WARWICK, R.M. 1999. The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Mar. Ecol.-Prog. Ser. 184:21-29, 10.3354/meps184021.
    » https://doi.org/10.3354/meps184021
  • COSTA, J.B.P., MELO, F.P.L., SANTOS, B.A. & TABARELLI, M. 2012. Reduced availability of large seeds constrains Atlantic forest regeneration. Acta Oecol. (Montrouge), 39:61-66, 10.1016/j.actao.2011.12.002.
    » https://doi.org/10.1016/j.actao.2011.12.002
  • DEAN, W. 1996. A ferro e fogo: a história e a devastação da Mata Atlântica brasileira. Companhia das Letras, São Paulo.
  • DOMĺNGUEZ, L.F., PRICE, J., OTTO, R. & FERNÁNDEZ-PALACIOS, J.M. 2010. Using taxonomic and phylogenetic evenness to compare diversification in two Island Floras. Perspect. Plant. Ecol. 12(2):93-106, 10.1016/j.ppees.2009.12.001.
    » https://doi.org/10.1016/j.ppees.2009.12.001
  • FERRAZ, E.B.N., ARAÚJO, E.L. & SILVA, S.I. 2004. Floristic similarities between lowland and montane areas of Atlantic Coastal Forest in Northeastern Brazil. Plant Ecol. 174(1):59-70, 10.1023/B:VEGE.0000046062.77560.f5.
    » https://doi.org/10.1023/B:VEGE.0000046062.77560.f5
  • FIASCHI, P. & PIRANI, J.R. 2009. Review of plant biogeographic studies in Brazil. J. Syst. Evol. 47(5): 477-496, 10.1111/j.1759-6831.2009.00046.x.
    » https://doi.org/10.1111/j.1759-6831.2009.00046.x
  • FREYRE, G. 2004. Nordeste: aspectos da influência da cana sobre a vida e a paisagem do Nordeste do Brasil. 7 ed. Global Editora, São Paulo.
  • FUNDAÇÃO SOS MATA ATLÂNTICA/INPE. 2005. Atlas dos remanescentes florestais da Mata Atlântica no período de 2000-2005. Fundação SOS Mata Atlântica/INPE, São Paulo.
  • GENTRY, A.H. & DODSON, C. 1987. Contribution of Nontrees to Species Richness of a Tropical Rain Forest. Biotropica 19(2):149-156.
  • GENTRY, A.H. 1992. Tropical Forest Biodiversity: Distributional Patterns and Their Conservational Significance. Oikos 63(1):19-28.
  • GIULIETTI, A.M., HARLEY, R.M., QUEIROZ, L P., WANDERLEY, M G.L. & VAN DEN BERG C. 2005. Biodiversity and Conservation of Plants in Brazil. Conserv. Biol. 19(3):632-639, 10.1111/j.1523-1739.2005.00704.x.
    » https://doi.org/10.1111/j.1523-1739.2005.00704.x
  • GORENSTEIN, M.R. 2009. Diversidade de espécies em comunidades arbóreas: aplicações de índices de distinção taxonômica em três formações florestais do Estado de São Paulo. Tese de doutorado. Piracicaba: Universidade de São Paulo.
  • GWALI, S., OKULLO, P., HAFASHIMANA, D. & BYABASHAIJA, D.M. 2010. Taxonomic diversity, distinctness, and abundance of tree and shrub species in Kasagala forest reserve in Uganda: implications for management and conservation policy decisions. Trop. Conserv. Sci. 3(3):319-333.
  • IVANAUSKAS, N.M. & RODRIGUES, R.R. 2000. Florística e fitossociologia de remanescentes de floresta estacional decidual em Piracicaba, São Paulo, Brasil. Rev. Bras. Bot. 23(3):291-304, 10.1590/S0100-84042000000300005.
    » https://doi.org/10.1590/S0100-84042000000300005
  • HAMMER, Ø., HARPER, D.A.T., & RYAN, P D. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electr. 4(1): 1-9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm(último acesso em 16/04/2012).
    » http://palaeo-electronica.org/2001_1/past/issue1_01.htm
  • HIETZ, P., BUCHBERGER, G., WINKLER, M. 2006. Effect of forest disturbance on abundance and distribution of epiphytic bromeliads and orchids. Ecotropica 12(2):103-112.
  • IUCN. 2013. IUCN Red List of Threatened Species. Version 2011.2.www.iucnredlist.org (último acesso em 06/03/2013).
    » www.iucnredlist.org
  • JERUSALINSKY, L., OLIVEIRA, M.M., PEREIRA, R.F., SANTANA, V., BASTOS, P.C. &, FERRARI, S F. 2006. Preliminary evaluation of the conservation status of Callicebus coimbrai Kobayashi & Langguth, 1999 in the Brazilian state of Sergipe. Primate Cons. 21:25-32, 10.1896/0898-6207.21.1.25.
    » https://doi.org/10.1896/0898-6207.21.1.25
  • LANDIM, M.F. & LANDRUM, L.R. 2002. The genusCampomanesia (Myrtaceae) in atlantic rain forest fragments in Sergipe, Northeast region of Brazil. Sida 20(1):205-214.
  • LANDIM, M.F. & SIQUEIRA, E.R. 2001. Caracterização florística e ecológica da mata atlântica de Sergipe In Mata Atlântica de Sergipe (E.R. Siqueira, F.E. Ribeiro, orgs). Embrapa Tabuleiros Costeiros, Aracaju, p. 9-50.
  • LANDRUM, L.R. & KAWASAKI, M.L. 1997. The genera of Myrtaceae in Brazil: an illustrated synoptic treatment and identification keys. Brittonia 49(4):508-536, 10.2307/2807742.
    » https://doi.org/10.2307/2807742
  • LAURANCE, W.F., FERREIRA, L.V., RANKIN-DE MÉRONA, J., LAURANCE, S.G., HUTCHINGS, R.G. & LOVEJOY, T.E. 1998. Effects of forest fragmentation on recruitment patterns in Amazonian tree communities. Conserv. Biol. 12(2):460-464, 10.1046/j.1523-1739.1998.97175.x.
    » https://doi.org/10.1046/j.1523-1739.1998.97175.x
  • LAURANCE, W.F., DELAMÔNICA, P., LAURANCE, S.G., VASCONCELOS, H.L. & LOVEJOY, T.E. 2000. Rainforest fragmentation kills big trees. Nature 404(6780):836-836, 10.1038/35009032.
    » https://doi.org/10.1038/35009032
  • TABARELLI, M., MANTOVANI, W. & PERES, C.A. 1999. Effects of habitat fragmentation on plant guild structure in the montane Atlantic forest of southeastern Brazil. Biol. Conserv. 91(2-3):119-127, 10.1016/S0006-3207(99)00085-3.
    » https://doi.org/10.1016/S0006-3207(99)00085-3
  • LEITÃO FILHO, H.F., 1987. Considerações sobre a florística de florestas tropicais e sub- tropicais do Brasil. I. Pesq. Estud. For. 35:41-46.
  • LIMA, H.C. DE QUEIROZ, L.P.,, MORIM, M.P., SOUZA, V.C., DUTRA, V.F., BORTOLUZZI, R.L.C., IGANCI, J.R.V., FORTUNATO, R.H., VAZ, A.M.S.F., SOUZA, E.R.DE., FILARDI, F.L.R., VALLS, J.F.M., GARCIA, F.C.P., FERNANDES, J.M., MARTINS-DA-SILVA, R.C.V., PEREZ, A.P.F., MANSANO, V.F., MIOTTO, S.T.S., TOZZI, A.M.G.A., MEIRELES, J.E., LIMA, L.C.P., OLIVEIRA, M.L.A.A., FLORES, A.S., TORKE, B.M., PINTO, R.B., LEWIS, G.P., BARROS, M.J.F., SCHÜTZ, R., PENNINGTON, T., KLITGAARD, B.B., RANDO, J.G., SCALON, V.R., CARDOSO, D.B.O.S., COSTA, L.C.DA, SILVA, M.J.DA, MOURA, T.M., BARROS, L.A.V, L.A.V.DE, SILVA, M.C.R., QUEIROZ, R.T., SARTORI, A.L.B., CAMARGO, R.A. & LIMA, I.B. 2013. Fabaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. (http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB115) (último acesso em 15/07/2013).
    » http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB115
  • LINARES-PALOMINO, R., CARDONA, V., HENNIG, E.I., HENSEN, I., HOFFMANN, D., LENDZION, J.S., SOTO, D., HERZOG, S.K. & S K. & KESSLER, M. 2009. Non-woody life form contribution to vascular plant species richness in a tropical American forest. Plant Ecol. 201(1):87-99, 10.1007/s11258-008-9505-z.
    » https://doi.org/10.1007/s11258-008-9505-z
  • LISTA DE ESPÉCIES DA FLORA DO BRASIL. 2014. http://floradobrasil.jbrj.gov.br/jabot/listaBrasil/ConsultaPublicaUC/ConsultaPublicaUC.do(último acesso em 14/03/2014).
    » http://floradobrasil.jbrj.gov.br/jabot/listaBrasil/ConsultaPublicaUC/ConsultaPublicaUC.do
  • MARQUES, M.C.M, SWAINE, M.D. & LIEBSCH, D. 2011. Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic Forest. Biodivers. Conserv. 20(1):153-168, 10.1007/s10531-010-9952-4.
    » https://doi.org/10.1007/s10531-010-9952-4
  • MCVAUGH, R. 1968. The genera of American Myrtaceae - an interim report. Taxon 17(4):354-418.
  • MELASTOMATACEAE.NET. 2013. A Site with Information on the Biodiversity of Melastomataceae. (http://www.melastomataceae.net/) (último acesso em 16/07/2013).
    » http://www.melastomataceae.net/
  • MORI, S.A, SILVA, L.M., LISBOA, G. & CORADIN, L. 1989. Manual de herbário fanerogâmico. Centro de Pesquisa do Cacau, Ilhéus.
  • MUELLER-DOMBOIS, D. & ELLENBERG H. 1974. Aims and methods of vegetation ecology. Wiley, New York.
  • MURRAY-SMITH, C., BRUMMITT, N.A., OLIVEIRA FILHO, A.T, BACHMAN, S, MOAT, J., LUGHADHA, E.M.N & LUCAS, E.J. 2008. Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conserv. Biol. 23(1):151-163, 10.1111/j.1523-1739.2008.01075.x.
    » https://doi.org/10.1111/j.1523-1739.2008.01075.x
  • MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403 (6772):853-858
  • NASCIMENTO, L.M., RODAL, M.J.N. & SILVA, A.G. 2012. Florística de uma floresta estacional no Planalto da Borborema, nordeste do Brasil. Rodriguésia 63(2):429-440.
  • OLIVEIRA FILHO, A.T & FONTES, M.A.L. 2000. Patterns of floristic differentiation among Atlantic Forest in South-Eastern Brazil and the influence of climate. Biotropica 32(4b):793-810.
  • OLIVEIRA, M.A., GRILLO, A. & TABARELLI, M. 2005. Levantamento Florístico dos Fragmentos Florestais da Usina Serra Grande, Alagoas. Relatório Técnico, Centro de Pesquisas Ambientais do Nordeste, Recife. Disponível em: http://cepan.org.br/uploads/file/arquivos/c2140c7bf307f4387d5b34665731b88c.pdf
    » http://cepan.org.br/uploads/file/arquivos/c2140c7bf307f4387d5b34665731b88c.pdf
  • OLIVEIRA, V.B., PAGLIA, A.P., FONSECA, M. & GUIMAR S, E. 2010. RPPN e biodiversidade: o papel das reservas particulares na Proteção da biodiversidade da Mata Atlântica. Belo Horizonte: Conservação Internacional ߓão Paulo: Fundação SOS Mata Atlântica ߃uritiba: The Nature Conservancy, 2010.
  • PEIXOTO, G.L., MARTINS, S.V., SILVA, A.F. & SILVA, E. 2004. Floristic survey of the tree layer in na area of Atlantic Rainforest in Serra da Capoeira Grande Environmental Protection Area, Rio de Janeiro State, Brazil. Acta Bot. Bras. 18(1):151-160, 10.1590/S0102-33062004000100013.
    » https://doi.org/10.1590/S0102-33062004000100013
  • PEREIRA, M.S & ALVES, R.R.M. 2006. Composição florística de um remanescente de Mata Atlântica na área de Proteção Ambiental Barra do Rio Mamanguape, Paraíba, Brasil. Rev. Bras. Ciênc. Terra 6(1):357-366.
  • PRATA, A.P.N., AMARAL, M.C.E., FARIAS, M.C.V. & ALVES, M.V. 2013. Flora de Sergipe. 1a ed. Aracaju: Gráfica e Editora Triunfo.
  • PROENÇA, C.E.B., LANDIM, M.F. & OLIVEIRA, M.I.U. 2013. Myrtaceae. In Flora de Sergipe (Prata, A.P.N., Amaral, M.C.E., Farias, M.C.V. & Alves, M.V., orgs.). Gráfica e Editora Triumfo, Aracaju, p.364-430.
  • PRATA, A.P.N., AMARAL, M.C.E., FARIAS, M.C.V., ALVES, M. 2013. Flora de Sergipe. 1. ed. Aracaju: Gráfica e Editora Triunfo. 592p .
  • PRIMACK, R.B. & RODRIGUES, E. 2001. Biologia da Conservação. Editora Planta, Curitiba.
  • RANTA, P., BROM, T., JOENSUU, E. & MIKKO, S. 1998. The fragmented Atlantic forest of Brazil: size, shape and distribution of forest fragments. Biodivers. Conserv. 7(3):385-403, 10.1023/A:1008885813543.
    » https://doi.org/10.1023/A:1008885813543
  • REVEAL, J.L. & CHASE, M.W. 2011. APG III: Bibliographical Information and Synonymy of Magnoliidae. Phytotaxa 19(1):71-134.
  • RIBEIRO, M.C., METZGER, J.P., MARTENSEN, A.C., PONZONI, F.J. & HIROTA, M.M. 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142:1141-53, 10.1016/j.biocon.2009.02.021.
    » https://doi.org/10.1016/j.biocon.2009.02.021
  • RODAL, M.J.N., LUCENA, M.F.A., ANDRADE, K.V.S.A. & MELO, A.L. 2005. Mata do Toró: uma floresta estacional semidecidual de terras baixas no nordeste do Brasil. Hoehnea 32(2):283-294.
  • ROLIM, S.G., IVANAUSKAS, N.M., RODRIGUES, R.R., NASCIMENTO, M.T., GOMES, J.M.L., FOLLI, D.A. & COUTO, H.T.Z. 2006. Composição Florística do estrato arbóreo da Floresta Estacional Semidecidual na Planície Aluvial do rio Doce, Linhares, ES, Brasil. Acta bot. bras. 20(3):549-561, 10.1590/S0102-33062006000300005.
    » https://doi.org/10.1590/S0102-33062006000300005
  • RICHARDS, P.W. 1996. The tropical rain forest: An ecological study, second edition. Cambridge University Press, Cambridge. 575 pp.
  • SCHNITZER, S.A. & BONGERS, F. 2002. The ecology of lianas and their role in forests. Trends Ecol. Evol. 17(5):223-230, 10.1016/S0169-5347(02)02491-6.
    » https://doi.org/10.1016/S0169-5347(02)02491-6
  • SILVA, I.A. & BATALHA, M.A. 2006. Taxonomic distinctness and diversity of a hyper seasonal savanna in central Brazil. Divers. Distrib. 12(6):725-730, 10.1111/j.1472-4642.2006.00264.x.
    » https://doi.org/10.1111/j.1472-4642.2006.00264.x
  • SOBRAL, M., PROENÇA, C., SOUZA, M., MAZINE, F. & LUCAS, E. 2013. Myrtaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/2012/FB010334 (último acesso em 16/04/2013).
    » http://floradobrasil.jbrj.gov.br/2012/FB010334
  • STEHMANN, J.R., FORZZA, R.C., SOBRAL, M. & KAMINO, L.H.Y. 2009. Gimnospermas e Angiospermas. In Plantas da Floreta Atlântica. (J. R.Stehmann, R. C. Forzza, A. Salino, M. Sobral, D. P.Costa & L. H. Y. Kamino, eds), Jardim Botânico do Rio de Janeiro, Rio de Janeiro, p.27-37.
  • TABARELLI, M. & MANTOVANI, W. 1999. A riqueza de espécies arbóreas na floresta atlântica de encosta no estado de São Paulo (Brasil). Rev. Bras. Bot. 22(2):217-223, 10.1590/S0100-84041999000200012.
    » https://doi.org/10.1590/S0100-84041999000200012
  • TABARELLI, M., PINTO, L.P., SILVA, J.M.C., HIROTA, M.M., & BEDÊ, L.C. 2005. Desafios e oportunidades para a conservação da biodiversidade na Mata Atlântica brasileira. Megadiversidade 1(1):132-138.
  • TABARELLI, M., AGUIAR, A.V., GRILLO, A. DA S. & SANTOS, A.M.M. 2006. Fragmentação e perda de habitats na Mata Atlântica ao norte do Rio São Francisco. In Fragmentos de Mata Atlântica do Nordeste - Biodiversidade, Conservação e suas Bromélias (Siqueira-Filho, C. & Leme, E.M.C., orgs), Rio de Janeiro: Andrea Jakobsson Estúdio. Pp. 80-99.
  • TABARELLI, M., DA SILVA, J.M.C., & GASCON, C. 2004. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodiversity & Conservation, 13(7), 1419-1425, 10.1023/B:BIOC.0000019398.36045.1b.
    » https://doi.org/10.1023/B:BIOC.0000019398.36045.1b
  • TOLIMIERI, N., & ANDERSON, M.J. 2010. Taxonomic distinctness of demersal fishes of the California current: moving beyond simple measures of diversity for marine ecosystem-based management. PloS One 5(5) e10653:1-14.
  • THE PLANT LIST. 2013. http://www.theplantlist.org (último acesso em 05/05/2013).
    » http://www.theplantlist.org
  • VEIGA, L.M., SOUSA, M.C., JERUSALINSKY, L., FERRARI, S.F., DE OLIVEIRA, M.M., SANTOS, S.S.D., VALENTE, M.C.M. & PRINTES, R.C. 2008.Callicebus coimbrai In IUCN 2008. IUCN Red List of Threatened Species. www.iucnredlist.org (último acesso em 11/03/2012).
    » www.iucnredlist.org
  • WEBB, C.O. 2000. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am. Nat. 156(2):145-155, 10.1086/303378.
    » https://doi.org/10.1086/303378
  • ZIPPARRO, V.B., GUILHERME, F.A.G., ALMEIDA-SCABBIA, R.J. & PATRĺCIA, L.C. 2005. Levantamento florístico de floresta atlântica no sul do estado de São Paulo, Parque Estadual Intervales, Base Saibadela. Biota Neotrop. 5(1):1-24 http://www.biotaneotropica.org.br/v5n1/pt/abstract?inventory+BN02605012005(último acesso em 16/04/2012)., 10.1590/S1676-06032005000100015
    » https://doi.org/10.1590/S1676-06032005000100015» http://www.biotaneotropica.org.br/v5n1/pt/abstract?inventory+BN02605012005

Publication Dates

  • Publication in this collection
    Mar 2015

History

  • Received
    11 Sept 2013
  • Reviewed
    19 Sept 2014
  • Accepted
    1 Oct 2014
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