Diversity of the Ant Genus Neoponera Emery , 1901 ( Formicidae : Ponerinae ) in the North of the Brazilian Atlantic Forest , with New Records of Occurrence

The Brazilian Atlantic Forest is considered a global conservation hotspot (Myers, 2000; Mittermeier et al., 2005), as it is one of the richest biomes in biodiversity as well as one of the most threatened on the planet, since only 12.4% of forest remnants remain compared to the original coverage of 1,315,460 km2 in the 16th Century (SOS Mata Atlântica, 2018; INPE, 2018). With this significant reduction of its original coverage, the current landscape of the Atlantic Forest is composed by a mosaic of native vegetation fragments and crop areas, including forest remnants of over 3 hectares of different shapes and sizes, of these two main forest formations: Abstract Composed of two main forest formations, Ombrophilous Forest and Seasonal Forest, the Brazilian Atlantic Forest biome is constituted currently by a mosaic of forest remnants and secondary vegetation. Representatives of the Ponerinae ant genus Neoponera are observed mainly in both wet and seasonally dry forests. The aim of this study was to approach the diversity of the genus Neoponera in the north of the Atlantic Forest of Brazil (from the extreme north of its distribution to the Doce River hydrographic basin in the south), associating the occurrence of ant species with the types of vegetation. We have compiled occurrence data from the collection of the Myrmecology Laboratory of the Cocoa Research Center, on internet, or available in literature. We found information on 23 species of Neoponera, including a new record for the Atlantic Forest, Neoponera globularia (Mackay & Mackay, 2010), and a new record for Brazil, Neoponera fiebrigi Forel, 1912. The relative composition of the Neoponera assemblages was evaluated according to the types of vegetation. We found that the occurrence of the genus Neoponera is mainly related to the types of vegetation of the focus region, principally dense forests where a higher diversity was observed. Sociobiology An international journal on social insects


Introduction
The Brazilian Atlantic Forest is considered a global conservation hotspot (Myers, 2000;Mittermeier et al., 2005), as it is one of the richest biomes in biodiversity as well as one of the most threatened on the planet, since only 12.4% of forest remnants remain compared to the original coverage of 1,315,460 km 2 in the 16th Century (SOS Mata Atlântica, Ombrophilous Forest and Seasonal Forest (Ribeiro et al., 2009;Tabarelli et al., 2010;SOS Mata Atlântica, 2018;INPE, 2018;MMA, 2018). In perennial ombrophilous forests, the incidence of sunlight is low at the lower strata and the trees are tall; on the other hand, in semideciduous or deciduous seasonal forests, a considerable part of the foliage is lost during the dry season, which favors the penetration of sunlight until the floor, contributing to the formation of a more open vegetation structure with few epiphytes (Pereira, 2009;Colombo & Joly, 2010).
Studies on the structure and composition of animal and plant communities are essential for the recovery and preservation of forest remnants (Ferreira et al., 2018), as well as for the conservation of biological diversity. However, we must understand first the main patterns of their geographic distribution to carry out these studies (Papes & Gaubert, 2007;Sigrist & Carvalho, 2008). In view of their high diversity and sensitivity to changes in the physical and biological environment, the insects, especially the ants (Hymenoptera: Formicidae), are useful for such studies (Santos et al., 2006;Ribas et al., 2012;Schmidt et al., 2013). Some ants directly or indirectly control the availability of resources, changing the state of biotic or abiotic conditions for other organisms (Jones et al., 1997). Their role as ecosystem engineers, coupled with their abundance in terrestrial ecosystems, reveals the ecological importance of this group (Folgarait, 1998). These ants contribute to structure the environment through soil ventilation and nutrient cycling, seed dispersal, mutualistic associations with plants and animals, on evolutionary as well as ecological scales (Moreau et al., 2006;Klimes et al., 2012;Dejean et al., 2014).
Ponerinae is one of the most diverse groups within Formicidae with regard to morphology and behavior. In this subfamily, Neoponera is the second more genus in the Neotropical Region (after Leptogenys) with 57 species Schmidt & Shattuck, 2014), occurring from southern Texas and northern Mexico to northern Argentina and southern Brazil . To date, 35 species of Neoponera have been recorded in Brazil , with representatives found throughout the country, preferably in humid forests, at ground level or in trees, but also in dry forests with seasonal rainfall (Lattke, 2003;. Ants of the genus Neoponera generally are much more frequent in conserved areas than in anthropized lands (Campiolo et al., 2015). This fact strongly suggests that a set of information on the distribution of this group can help in monitoring environment quality and, furthermore, will provide valuable arguments to justify policies aiming at the implantation of conservation units. Although the pattern of global ant diversity is similar to that of other taxa (for example, vascular plants), many regions have much less recorded diversity than expected. This can be related to several factors, including climate change and migration, emphasizing that regions with still unknown diversity are often the regions where deforestation is occurring most rapidly (Guénard et al., 2012), such like the Atlantic Forest. The present study aimed to analyze the current diversity for the Neoponera genus in the northern part of the Brazilian Atlantic Forest biome, inserting new records, evaluating the richness and the association of Neoponera species with different forest formations (types of vegetation) within the biome.
We defined the Doce River as the southern geographic boundary to outline the studied area, which is the northern part of the Brazilian Atlantic Forest (Fig 1). The Doce River is one of the larger Brazilian rivers and its hydrographic basin presents a worrying picture of environmental degradation, since it is within the limits of two global biodiversity hotspots, 98% of its area is in the Atlantic Forest and the remaining 2% in the Cerrado (Mittermeier et al., 2005;Azevedo-Santos et al., 2016;Pires et al., 2017). The Doce River flows 888 km and its basin has an area of about 84,000 km 2 , of which 86% are in the state of Minas Gerais and 14% in that of Espírito Santo. It is considered as an effective biogeographical barrier at least since the Pleistocene (Carnaval & Moritz, 2008). Thus, the analyzed area covers from the Southeast of Brazil, from the north of Espírito Santo and part of Minas Gerais, to the Northeast of the country, and includes the states of Bahia, Sergipe, Alagoas, Pernambuco, Paraíba and Rio Grande do Norte. In the Northeast, the biome is limited to the Caatinga and in the Southeast, to the Cerrado (Pereira, 2009). In general, it presents precipitation index above 1,000 mm 3 per year and several climatic types, such as humid tropical, hot and super humid, tropical altitudinal and mesothermal climates according to the Köppen-Geiger classification (Pereira, 2009).

Data collection
Neoponera species data were set up from the Myrmecology Laboratory collection of the Cocoa Research Center (CPDC), at Ilhéus-BA, Brazil, looking for information on specimen collection locations and geographic coordinates. Occurrence data were also compiled from the online data networks Antweb.org (accessed on 2018/2019) and Antmaps. org (accessed on 2018/2019). Another search was performed based on literature, using the species names as keywords. We consider the possibility that the species was registered with an outdated name, especially when included in the genus Pachychondyla before the revision of this genus by Schmidt and Shattuck (2014). We reviewed information about these species across Brazil and, subsequently, analyze their distribution in the north of the Brazilian Atlantic Forest biome to compile the list of species and data (reference codes are available in Table 5).

Statistical analysis
We built a spreadsheet with data compiled for the occurrence of species recorded in different locations in the north of the Atlantic Forest biome. We assessed the structure of Neoponera assemblages according to the types of vegetation (Table 1; Fig 1). For that purpose, we evaluated the similarity of Neoponera assemblages (species presence/absence) according the vegetation types using the Jaccard's index. In addition, the association between species and vegetation types was illustrated using a multidimensional non-metric ordering (NMDS) using the Bray-Curtis index. These analyzes were performed using the software R v. 3.6.1(R Development Core Team 2019).

Results
The total number of records of the survey comprises 23 species (Table 2) of Neoponera, distributed in the Atlantic Forest above the geographical boundary of Doce River (Tables 3 and  4). Between these, Neoponera globularia ) is a new record for the Atlantic Forest, and Neoponera fiebrigi Forel, 1912 a new record for Brazil. We also found records of Neoponera goeldii Forel, 1912 (species previously known from the Amazonian biome only) in the state of Bahia at least at 1,500 km further east from the nearest record.
The types of vegetation that presented a higher number of species of Neoponera were: VS-AA.D (19 spp.), VS-AA.C (10) VS-AA.F (7) and SO (6). The number of species in the other types of vegetation varied from one to three (Fig 2). Three vegetation types presented only a single species: VS-AA.A and Db (N. apicalis) and AA-SN (N. villosa) (Fig 2).
When we test the similarity between vegetation types according to the presence/absence of Neoponera species, we observed that Db and VS-AA.A share the same assemblages (Fig 3). In general, the other types of vegetation present low similarity between them (less than 50%), especially VS-AA.D and VS-AA.C (about 40% of similarity). It is worth noting that the assemblages found in vegetation types Pf and AA.P (38% similarity between them) have low similarity with the other vegetation types (Fig 3).

Discussion
So far 35 species were recorded for the Neoponera genus in Brazil . With this survey and insertion of new records and occurrences, this number can be updated to 36 species, 23 of which are found in the northern part of the Atlantic Forest biome. Thus, N. fiebrigi, previously registered only in Paraguay, Argentina ) and Panama (Schmidt & Schattuck, 2014), constitutes a new record for Brazil and the Atlantic Forest.
We observed that the occurrence of many species of the genus Neoponera in the Brazilian Atlantic Forest is related to dense vegetation, such like secondary forests or vegetation at climax. These environments offer a higher number of records and species richness than opened environments. The same was observed by Campiolo et al. (2015) in a study that points out the Ponerinae preferences for forest-type habitats with dense vegetation cover. These characteristics results from the particular habitat requirements of each species of the genus.
For example, N. apicalis, N. villosa, N. carinulata, N. crenata, N. curvinodis and N. inversa are arboreal . Some species can also nest in undergrowth, trunks and hollow branches fallen on the ground, where moisture and shade conditions are suitable, such as for example, N. verenae (Delabie et al., 2008, Araujo et al., 2019. The species recorded in a higher number of vegetation types, N. apicalis, is known to occur in both primary and secondary moist forests . However, Delabie et al. (2008) suggest that the apicalis group of Neoponera (sensu Wild, 2005) is in fact a complex of at least nine cryptic species, including N. apicalis, N. obscuricornis and N. verenae (Ferreira et al., 2010), which could explain the range of habitats chosen by the ants.
The type of vegetation with the higher diversity of Neoponera was the Ombrophilous Dense Forest. This kind of forests presents moist soil covered by a thick layer of leaf-litter (Pereira, 2009). Because it uses to be more heterogeneous in diversified environments, the leaf-litter offers certainly a range of niches and, as a result, a well-diversified community of soil fauna; in addition, we can expect that the greater the amount of leaf-litter, the greater the availability of resources, such as food and nesting sites (Santos et al., 2006;Ferreira et al., 2018). However, the seasonal deciduous and semideciduous forests, which occur in places with 2 to 5 months of dry season (Colombo & Joly, 2010), also showed a relatively high species richness. Lattke (2003) had already pointed out that some Neoponera species are able to colonize dry forest areas with a marked rainfall regime.
Our observations point out some particularities such as the occurrence of N. goeldii in the Atlantic Forest biome, with an extremely reduced population living isolated in the Península de Maraú, Bahia (J.H.C. Delabie, personal communication, December, 2019), while this species is common in Amazon . In fact, there are numerous physiographic, floristic, fauna and climatic similarities between the Atlantic Forest biome, in the coastal strip which runs from the south of the state of Bahia to the north of the state of Espírito Santo ("Central Corridor of the Mata Atlântica"), and the Amazon Forest (Pereira, 2009). According to Joly et al. (1999), the occurrence of species typical of the Amazon region in the Atlantic Forest of southern Bahia confirms that these biomes have undergone expansion and retraction processes during the Pleistocene climatic fluctuations. In other words, at one or several intervals in this period, transition bridges occurred allowing the arrival of typically Amazonian species in the Atlantic Forest biome (Ab'Saber, 2003;Costa, 2003).
The ant species Neoponera globularia, N. goeldii, N. laevigata, N. schultzi and N. venusta      together with N. concava, which likewise predominates in dense forest, are endemic from Brazil . In the Atlantic Forest, four areas of endemism are reported (Silva et al., 2004;Sigrist & Carvalho, 2008;Peres et al., 2020), and three of which are considered in our area of study: i) Central Bahia, ii) Central Corridor of the Atlantic Forest, and iii) Pernambuco. These are biogeographic regions supported by several taxonomic groups, being a valid representation of regionalization for studies and conservation of biodiversity (Peres et al., 2020). The Neoponera data obtained in our study basically comprise records for the Central Corridor of the Atlantic Forest, an area of endemism that extends from the south of the state of Bahia to the north of Espírito Santo, with N. schultzi being an endemic species of that region. Thus, we understand that the occurrences of ants reinforce the importance of the conservation of these ants in the Central Corridor of the Atlantic Forest. Some studies carried out in the Atlantic Forest (Santos et al., 2006;Silva et al., 2007) have shown that ant communities use to be affected by anthropogenic disturbances. It is expected that in areas where landscape fragmentation is dominant and land use is excessive and disordered, many species will not be able to face climatic changes and migrate at a sufficient rate to maintain their population (Pearson & Dawson, 2003).

State
County Coordinate Vegetation type Code Table 5. References of the data sources used in the study.
Since ants are organisms faithful for a specific type of habitat, and may allow inferences about the rehabilitation of an area (Schmidt et al., 2013), the occurrence of some Neoponera in more than a single type of vegetation, like N. apicalis, N. villosa, N. bucki, N. curvinodis, Neoponera unidentata (Mayr, 1862) and N. inversa (Fig 4), strongly suggest the connectivity between vegetation types. Thus, the conservation of forest remnants and even some kinds of agriculture which maintains a forest structure (cocoa agroforestry, for example) can be decisive for the conservation of this group of ants (Delabie et al., 2007;Campiolo et al., 2015). Further studies should evaluate the relationships between the occurrence and distribution of the species of Neoponera and the habitat conservation including also the other areas covered by the biome.

Acknowledgments
This study is part of the requirements for the obtention of the first author's Master Degree. Thanks are due to the Programa de Pós-Graduação em Zoologia of State University of Santa Cruz (UESC). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES) -Finance Code 001. PSS acknowledges her study grant from CAPES; JHCD and CSFM thank CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for their research grants.