Floristic composition of Melastomataceae between reforested and natural areas in the Recife Atlantic Forest, Pernambuco, Brazil

Local extinction of native Atlantic Forest flora species occurs mainly due to habitat fragmentation. Reforestation and natural regeneration can mitigate these factors. The present study attempts to understand whether floristic composition and dispersal processes are being reestablished in an area of lowland Atlantic Forest, eight years after its reforestation. The study area was an old pasture set between two urban fragments in the city of Recife that was reforested in 2011. Melastomataceae species were collected in this area and the morphology of their fruits was compared with the species of the family recorded in the adjacent fragments. Miconia prasina, M. albicans, M. affinis, Clidemia hirta, and C. capitellata have been found in the reforested area. Although there are species with larger fruits in the adjacent fragments, there was no statistically significant


Introduction
Forest fragmentation is one of the main processes responsible for species extinction and the destruction of ecosystems (RIBEIRO et al., 2009), and is defined as the process of reducing a continuous landscape into subunits that differ from their matrix (FAHRIG, 2003). Fragmentation has profoundly affected the Atlantic Forest, originally the second largest rainforest in the Americas, spanning the Brazilian coast into Argentina and Paraguay and covering approximately 1.5 million km² (RIBEIRO et al., 2009). The Atlantic Forest is one of the main hotspots of biological diversity due to the drastic reduction of its original area and a great number of endemic species (MYERS et al., 2000;MITTERMEIER et al., 2003). Today, Atlantic Forest vegetation remains between 7% and 15% of its original coverage (RIBEIRO et al., 2009;REZENDE et al., 2018), while the north of the São Francisco River retains only 2% of its original vegetation (TABARELLI et al., 2006;RIBEIRO et al., 2009;REZENDE et al., 2018).
Successional changes affect species composition (LIEBSCH et al., 2008). Secondary successional stages favor pioneer and weedy species as a consequence of changes in light availability and temperature of microhabitats (OLIVEIRA et al., 2004;TABARELLI et al., 2004). During the natural regeneration process, a gradual replacement of small fruit species with larger fruit species is also expected (TABARELLI; PERES, 2002). Areas with a short recovery time present a predominance of species with fruit size that is considered small (on average 0.6 cm) and, as the area matures, there is a gradual substitution with larger fruit species (on average 1.5 cm) (TABARELLI; PERES, 2002). Based on these premises, one might expect that recently reforested areas present a predominance of small-fruited pioneer species in the understory.
Melastomataceae has about 4,500 species distributed in 150 genera that occur in tropical and subtropical zones worldwide (GOLDENBERG, 2012 Their species can disperse the seeds through biotic or abiotic vectors (REGINATO et al., 2020). When biotically dispersed, the species present fleshy berries that are dispersed by frugivorous birds and mammals (REGINATO et al., 2020).
Floristic studies have recorded 6 to 17 species of Melastomataceae in the Atlantic Forest remnants of the state of Pernambuco (MELO et al., 2011;CAVALCANTI et al., 2016). During the early stages of forest regeneration, Melastomataceae is the dominant family among small-sized fruit species from the Atlantic Forest above the São Francisco River (TABARELLI; PERES, 2002). Some studies reported that birds and marmosets consume fruits of the Melastomataceae species, confirming the importance of this family to the region's fauna (PONTES;SOARES, 2005;ALVES, 2014). This evidence reinforces the important role that the Melastomataceae plays in the Atlantic Forest above the São Francisco river, whether as a dominant element in the physiognomy, as a species-rich family, or as a source of food resource to the fauna.
In the present study, we investigate whether the floristic composition and dispersal processes are being reestablished in an area of lowland Atlantic Forest Floristic composition of Melastomataceae between reforested and natural areas eight years after reforestation. We expect to find a predominance of pioneer species of Melastomataceae in the understory of a reforested patch of Atlantic Forest since recently reforested areas could present similar dynamics to recently disturbed areas. Furthermore, if ecological processes are being reestablished, we will find a predominance of biotic dispersed species.

Study area
The area of study (reforested area -RA) is located in an intensely urbanized matrix that is part of the Curado District in Recife, Pernambuco, Brazil (8°04'40.9"S; 34°57'53.0"W), which is flanked by two remnants of the Lowland Atlantic Forest with areas of 9 and 30 ha (Matas do Curado -MC; Figure 1). It is adjacent to the Recife Botanical Garden in its western portion; in the southern portion is bordered by the Jardim Botânico Residential Complex, separated only by a wall; a fragment of the Atlantic Forest presenting the physiognomy of a mature fragment lies in the eastern portion , and is used by the surrounding communities, ; and the former Foundation of the Shopkeepers Club of Pernambuco, that once housed a municipal school system and is currently disabled, is located in the northern portion.
The climate of the region is tropical rainy (AS'); the dry season occurs in October, November, and December and the rainiest seasons are between May and July (NASCIMENTO et al., 2017). The average annual rainfall is 1,651 mm/year and the average temperature is 25°C. The soil of the region is classified as dystrophic red yellow argisols (NASCIMENTO et al., 2017). There are signs of anthropization in the area, especially on the north and south banks, seen in the presence of exotic orchard remnants and garbage disposal (NASCIMENTO et al., 2017). order to connect the fragments of MC through the RA.
In this reforestation, native tree species were used, but none of them belonged to Melastomataceae.

Data collection
Fieldwork was carried out from May 2018 to January 2019 and the collections were monthly. The dehydrated and processed materials were sent to the RB and UFP herbaria (acronyms according to THIERS, 2020). The collections were focused on the species of Melastomataceae. Their identification was based on specialized literature (CHAGAS, 2012; ARAÚJO; LIMA, 2013) and on the comparison of samples deposited in the UFP herbarium as well as with the types available on online platforms of Reflora Virtual Herbarium (http://reflora.jbrj.gov.br/reflora/ herbarioVirtual/) and SpeciesLink (http://www.splink. org.br/).
To compare whether the composition and richness of the RA are similar to that of MC, we also conducted collections on a MC and herbarium survey at the UFP. We complemented with a search on the SpeciesLink digital platform about the Melastomataceae species that occur in MC.
Data on fruit size and type for each species from both reforested and adjacent areas were obtained from taxonomic descriptions (CHAGAS, 2012; ARAÚJO; LIMA, 2013;) and measures from exsiccatae. In some cases, where there was no description of the fruit size and type in the taxonomic literature, measurements from exsiccates were taken. The classification of species according to dispersal syndrome was based on Van der Pijl (1982) and the successional classification was based on Gandolfi et al. (1995).

Data analysis
Species composition, richness, and categories were compared by simple descriptive statistics. To compare whether there is a difference in the fruit sizes between reforested and MC areas, a variance analysis and a Krustal-Wallis analysis were performed. Data analyzes were performed using the Past 3.19 software (HAMMER et al., 2001).

Results
In the MC fragment nine species of Melastomataceae and five species in the RA were found (Table 1). The fruits in the RA and MC areas are a fleshy berry type adapted to zoochoric dispersion. In the RA, all species were classified as pioneer (PI), typical of the Floristic composition of Melastomataceae between reforested and natural areas early stages of natural regeneration. The fruits in the RA are smaller than in the MC, 0.6 cm long and 0.7 cm long, respectively (Table 1), but there was no statistically significant difference between the means of the two areas (df = 1, F = 0.81, p = 0.38). Likewise, the medians showed no significant difference (H = 0.26, p = 0.59). Figure 2 shows the fruit of the most abundant species in the reforested area.

Discussion
The results show that the RA already presents expected ecological processes for a corridor between the two adjacent areas, acting as vectors for the colonization of native Atlantic Forest species. Even though the reforested area is smaller and more immature than the adjacent areas, the composition of native elements expected for phytophysiognomy is being established by natural processes.
All five Melastomataceae species found in the RA are categorized as pioneers, as expected for early regeneration stages in the Atlantic Forest (LIEBSCH et al., 2008). Pioneer species predominate in recently disturbed ecosystems (OLIVEIRA et al., 2004;TABARELLI et al., 2004). Liebsch et al. (2008) suggest that an Atlantic Forest patch needs 157 years for nonpioneer species to predominate. When we conducted the survey of Melastomataceae species the RA had presented less than 10 years of reforestation.
None of the species analyzed have anemochoric dispersion. The fruit morphology indicates that these species are consumed by animals which have been acting as dispersal vectors. This is reinforced by the fact that several genera of Melastomataceae are part of the diet of various animal groups (PONTES;SOARES, 2005;MARUYAMA et al., 2007;BARCELOS et al., 2013;ALVES, 2014;REGINATO et al., 2020). In addition, Melastomataceae has functional attributes that make species attractive to frugivorous animals, such as a large amount of fruit per plant and nutritional availability (MARUYAMA et al., 2007).
Birds are among the main dispersers of the Melastomataceae species, which may contribute differently to the quality and quantity of seed dispersal components BLAKE, 1999). Thus, different bird species may participate in some stages of dispersal, but not contribute equally in the process. For example, Ellison et al. (1993) observed that plant species from more open and bright environments tend to have a higher and faster germination rate when they pass through the digestive tract of birds than plant species from shaded environments. This pattern could explain the absolute predominance of the pioneer species of Melastomataceae in the area, even when considering that in adjacent fragments typical species of shaded environments can be found.
Some of the records of this relationship between fruit-eating birds and Melastomataceae species may be analogous to the events that are probably occurring in the RA. In a submontane rainforest fragment in northeastern Brazil, C. hirta and M. affinis were reported as part of the diet of the bird Chiroxiphia pareola Linnaeus, 1766 (ALVES, 2014). The C. pareola has populations in MC (PEREIRA et al., 2011). In a fragment of lowland Atlantic Forest in southeastern Brazil, two species of thrush (Turdus albicollis Vieillot, 1816 and Turdus amaurochalinus Cabanis, 1850) were found ingesting fruits and dispersing seeds of M. prasina (ALVES et al., 2008). Turdus amaurochalinus Cabanis, 1850 has been identified as one of the omnivorous avifauna species in forests adjacent to the regenerating area (PEREIRA et al., 2011).
In addition to birds, mammals also include the Melastomataceae species in their diets (REGINATO et al., 2020). The most correlated example of what is happening in the area is the record of a population of Callithrix jacchus Linnaeus, 1758 (White-tufted marmoset) from Dois Irmãos State Park using M. prasina in their diet, with the intake of the fruit gum (PONTES; SOARES, 2005). Notably, M. prasina is the most abundant species in the study area and with one of the largest fruits among the species studied. Similarly, the white-tufted marmoset has a particularly large population in the area, and it is easy to see that the various groups formed by moving and consuming the fruits of this and other species.
Fragmentation and urbanization of the northeastern Atlantic Forest caused an intense defaunation process of the region's relatively small and impoverished remnants (CANALE et al., 2012;GARBINO et al., 2018). However, our results provide a glimmer of hope for conservation of the region by demonstrating that natural processes can be reestablished in the northeastern Atlantic Forest.