An overview of the ant fauna (Hymenoptera: Formicidae) of the state of Maranhão, Brazil

The state of Maranhão, located in northeastern Brazil, comprises three biomes: Amazonian, Caatinga, and the Cerrado. To date, 99 ant species have been recorded in the literature from the state. In the present work, we provide for the first time a profile of the ant fauna in the state based on data from the historical literature and Brazilian institutional collections. The updated records on ant diversity for the state of Maranhão revealed a total of 279 species, belonging to 71 genera and 10 subfamilies. In total, 180 species are recorded for the first time in the state, of which four species recorded for the first time in Brazil. In summary, apart from documenting the ant fauna of the region, these results provide a basis for further studies and may contribute to future conservation efforts for the biomes present in this complex landscape. Key-Words. Distribution, Amazon, Caatinga, Cerrado, Checklist.


INTRODUCTION
Understanding the distribution of species is essential to determine regional and global patterns of biodiversity (Dalzochio et al., 2018). In this sense, taxonomic inventories contribute to characterize areas of endemism, reveal taxonomic novelties and improve scientific collections (Moura et al., 2014;Freitas et al., 2017). Further, the analysis of species distribution databases can help to identify gaps in sampling and species records, and can also be used in macroecological studies, species distribution modeling and to promote conservation strategies (Gasper et al., 2016).
Maranhão is a northeastern state in Brazil and comprises a total area of 329,642.170 km² (IBGE, 2018). Its political boundaries are the Atlantic Ocean to the north, the state of Tocantins to the south, the state of Piauí to the east, and the state of Pará to the west (Chaves et al., 2016). The state ISSN On-Line: 1807-0205 ISSN Printed: 0031-1049 ISNI: 0000-0004-0384-1825 is located in a heterogeneous landscape area under the influence of three biomes: Amazon, Cerrado, and the Caatinga. The vegetation cover -encompassing 14 different vegetation types -reflects the transition between super-humid and semi-arid climates (Santos et al., 2010;IBGE, 2018).
Similar to other states in Brazil, Maranhão has suffered with high human impact, mainly from the early 1960s, through the construction of highways, agricultural and mining projects (Celentano et al., 2017). Impacts include large-scale forest conversion to pasture or by "babaçu" palm trees (Orbignya phalerata Mart.) (Santos et al., 2010), and the expansion of agroindustry has converted large natural areas into grain crops (Brasil, 2009;Santos et al., 2010). In addition, other human activities, such as occupation, recreation and tourism (Chaves et al., 2016) have also a negative impact and have caused severe loss of biodiversity, resulting in drastic changes of the landscape.
The biodiversity of Maranhão is extremely diverse (Chaves et al., 2016;Desidério et al., 2017). Compared to other Brazilian states, however, the ant diversity is poorly known. The most recent information on ant species diversity in the state recorded 99 species, belonging to 37 genera and seven subfamilies (Janicki et al., 2016). This represents about ¼ of ant diversity in the state of Goiás and 35% of the ant species richness described for the state of Mato Grosso do Sul (Janicki et al., 2016), two other Brazilian states comparable in size to Maranhão.
Since the end of the 20 th century, collective efforts of several research groups, carring out inventories in different areas and employing complementary sampling methodologies, resulted in a significant increase in our knowledge about ant diversity in this state. Thus, the aim of this study is to present an updated list of the ant species in the state of Maranhão, considering recent field expeditions as well as material deposited in the main Brazilian ant collections. We also discuss some relevant aspects about the profile of the ant fauna, recovering the history of ant studies historically carried out in the state. Overall, our findings should be of great help in creating measures for species preservation and species recovery plans and represent the basis for future research.

Data from collections and literature
We listed material obtained from six Brazilian ant collections (Table 1), which have historically acted as main depositary institutions for samples collected in the state of Maranhão. We also compiled data from literature, including collection events focused on partial surveys of Maranhão ant fauna (Table 2).

Identifications and taxonomic validation
Ants were identified by the authors of the present study using taxonomic keys, comparing specimens with myrmecological collections, or by sending them to specialists (see "Acknowledgements"). The final list containing all specimens was verified by authors of this study (JAS, LPP and RMF). Species with dubious identification were carefully examined and, when necessary, have been removed from final data set.

Distribution and maps
The biomes present in Maranhão are the Amazon Forest, characterized by tall trees and periodic to permanently flooded plains; this biome is present in the north and, essentially, in the west portion of the state. The Cerrado covers the south, central and northeast areas of the state, formed by open grasslands (Cerrado aberto) to patches of dense vegetation (Cerradão). Finally, Maranhão presents a small and fragmented portion of
For the confirmation of sampled sites (Table 3) and maps preparation, the geographical coordinates, when not available on the specimens' label, were obtained from the IBGE (2011) or georeferenced using Google Earth Pro. In those cases, because we did not have access to the exact point of the sample site, we adapted a classification by the IBGE. Whenever the IBGE classified a municipality covering two biomes, we used the "transition" term after the government classification. For instance, the municipality of Imperatriz, which is classified by IBGE as "Amazon/Cerrado" biomes, becomes for the purpose of this study, "Amazon-Cerrado transition". For specific sites and localities for which names have been historically altered, we consulted Vanzolini & Papavero (1968) and Vanzolini (1992). The geographical records were mapped using QGIS v2.18.2 (QGIS Development Team, 2019).
The majority of records (214 species) was concentrated along the Amazon region, followed by the Cerrado (129 species), the Amazon-Cerrado transition regions (80 species) and finally the Cerrado-Caatinga transition region where only one species was recorded (Fig. 1). A total of 180 ant species were recorded for the first time in the state, and four species were recorded for the first time in Brazil (Table 4).

DISCUSSION
The first expeditions focused on studying the ant fauna of the state of Maranhão were performed in the late 1940s, with collections in the Cerrado areas undertaken by the myrmecologists Cincinnato Gonçalves and Walter W. Kempf. During the next three decades, collections by researchers, enthusiasts, and professional collectors had pursued the same goal -discovering new taxa and increasing the coverage of ants in scientific collections (Kempf, 1972a). Differently, from the 1980s until the beginning of the 21 st century, the main purpose of the expeditions was to carry out environmental impact assessment programs (Brandão et al., 2011). On the other hand, from the late 20 th century, with the hiring of researchers at universities in the state of Maranhão, several expeditions have been conducted focusing on ecological studies and reporting faunal inventories (Ramos et al., 2015;Gutiérrez et al., 2017;Silva et al., 2017).
Museums, scientific collections, and historical published literature all contain important information on species distributions recorded as presence data (Newbold, 2010). The accuracy of the distribution data is important for several applications in biology and for species conservation planning (Graham et al., 2008). Despite the concern to accurately document of species distribution that began in the first half of the 19 th century (Vanzolini, 2004), for the ants this occurred in the second half of the 20 th century. In the case of the records analysed in this work, the specific localities and geographic coordinates became available in the late 20 th century.
Not surprisingly, the data obtained from the ant literature clearly indicates that taxonomy is the discipline that most contributed to the knowledge of the ant fauna in the state. This is especially true for taxonomic revisions, which deal with large numbers of specimens (e.g., De Andrade & Baroni Urbani, 1999;Lattke, 2011). The high number of taxonomic publications in our survey is justified by the fact that this discipline was the first area of myrmecology to be developed in Brazil, allowing the formation of large repositories. However, although taxonomy is the discipline with the greatest number of published studies in relation to other areas, in the last 20 years the potential of ant fauna data has been explored in different study areas (Table 2).
Other factors that have contributed to increasing our knowledge of the ant fauna in the state of Maranhão are online tools, which provide high definition images of species (AntWeb, 2019), taxonomic literature (Bolton, 2019), geographic distribution of ant specimens (Janicki et al., 2016), and general information on ant taxa (AntWiki, 2019). These tools facilitate the identification of specimens and provide a fast and effective access to information. In addition, the improvement and development of collection methodologies (Figueiredo et al., 2013) has made the sampling more efficient.
Despite the increased understanding of biodiversity in this region, sampling coverage of ant fauna in Maranhão is strongly irregular (Fig. 1). Our study showed that the Amazon is the better sampled biome and also houses the largest number of species recorded in the state (Table 4). Most collection points are concentrated in the northern region of the state (Fig. 1), which corresponds to the Coastal region of Maranhão, with the highest population density (Chaves et al., 2016), and where the main research centers are located.
While the Cerrado, which corresponds to the biome with the highest coverage in the state (64%) (MMA, 2011;Stella, 2011), remains poorly sampled with extremely sparse collections (Fig. 1). In relation to this biome, it is in the southern part of the state where most of the collection points are concentrated, which in most cases came from samples derived from environmental impact assessment programs (e.g., Brandão et al., 2011).
The Amazon-Cerrado transition regions are also undersampled in the state, with few records available from taxonomic papers (Kempf, 1972a;Brandão, 1991) and collections. If we want to understand the association between species and forest formations it is essential to characterize species diversity in ecotones, as already observed by other groups (Santos et al., 2010;Maracahipes-Santos et al., 2018).
The Caatinga biome remains largely unknown in Maranhão, represented in our study by a single record in the Cerrado-Caatinga transition region (Fig. 1). Although the biome presents a small and fragmented spatial coverage (1% of the state territorial area) (Stella, 2011), the scarcity of information about the ant fauna in the Caatinga has also been observed in other regions of Brazil (Santos et al., 1999;Ulysséa & Brandão, 2013;Leal et al., 2017). This result illustrates the need for greater collection effort to understand and preserve biodiversity in the Caatinga and, consequently, in the state of Maranhão.
One of the main limitations of the data available to date on the ant fauna in Maranhão was a strong sampling bias, with most samples being collected near the main roads (Fig. 2). This pattern of biased sampling near highways, rivers, coasts, and cities has been reported in several taxonomic groups (Hijmans et al., 2000;Kadmon et al., 2003;Reddy & Dávalos, 2003;Newbold, 2010;Santos & Hoppe, 2018), which is explained by the ease access, researchers' interest in certain areas or taxa, and limited financial resources. However, further studies are required to reduce this sampling bias by using different collection methodologies and accessing previously unexplored sites.
Low levels of sampling in conservation areas of the state were also observed (Fig. 3). Conservation areas (i.e., national parks, ecological stations, extractive reserves, national forests, biological reserves, among others) are of fundamental importance for biodiversity conservation (Peres, 2005) and preserving ecosystem (Hallmann et al., 2017).
To the best of our knowledge, this is the first compilation focused on studying the ant fauna of Maranhão, one of the largest geopolitical regions of Brazil. Our study significantly increase the number of ant species recorded in the state and demonstrates the importance of carrying out planned inventories for a more detailed understanding of the regional ant fauna. Finally, our data provide the baseline information to further explore the ant fauna in Maranhão, to improve current knowledge and to accurately determine the occurrence of several species.

CONCLUSION
This paper represents an updated record of the ant species occurring in the state of Maranhão, with numbers increasing from 99 to 279 species. Further collection efforts in different biomes are essential for a better understanding of the biodiversity of the state, and for planning long-term conservation action. Ongoing studies on taxonomy, natural history, and ecology are certainly expected to contribute to this.