Ants of the Panga Ecological Station , a Cerrado Reserve in Central Brazil

Species lists are an invaluable tool for a more comprehensive analysis of diversity patterns. Such lists, when derived from a comprehensive sampling effort, can indicate the presence of rare, threatened, or ecologically important species. This study aimed to generate a species list of the ants of the Panga Ecological Station, a protected Cerrado reserve in southeastern Brazil. This list was generated through taxonomic identification or through unification of the morphospecies codes of all specimens collected at the reserve in ten different studies since 2003. Information about the types of habitat and strata of occurrence of each species or morphospecies was also compiled. The data presented here represents one of the most intensive ant inventories conducted in the Brazilian Cerrado . We recorded 277 ant species belonging to 58 genera and nine subfamilies. This number is 1.63 to 3.69 times higher than the number of species recorded in other Cerrado localities surveyed so far. More species were collected in the savanna (249 species) than in the forest habitats (108 species), and more species were collected on ground (226 species) than in arboreal vegetation (117 species). Taxonomic identification was possible for 171 of the 277 species collected. Three of the named species are recorded for the first time in Brazil. Among the 106 unidentified species, at least six of them represent new, undescribed species. Together, these results highlight the conservation potential of this Cerrado reserve.


Introduction
One of the first steps for the establishment of effective conservation actions and monitoring programs is the generation and maintenance of species distribution records (Agosti & Alonso, 2000).In this sense, species lists play an important role because they provide essential data for a more comprehensive analysis of diversity patterns, including biogeographical patterns (Fisher, 2010).The compilation of species lists can also determine the presence of rare, threatened, or ecologically important species (Agosti & Alonso, 2000) that otherwise could be missed in a single survey.In addition, recording the distribution of species is essential for the creation of a data network (Agosti & Alonso, (Fittkau & Klinge, 1973;Alonso & Agosti, 2000).Ants are a particularly important group of terrestrial invertebrates, as they establish mutualistic associations with many organisms (Ness et al., 2010), are predators of other invertebrates (Philpott & Armbrecht, 2006), secondary seed dispersers, and contribute to soil aeration (Lee & Foster, 1991) and nutrient cycling (Hudson et al., 2009).However, as is also the case for many other invertebrate groups, one of the difficulties in generating a list of ant species from a given locality or region is the taxonomic identification.This identification is usually performed at the "morphospecies" level, what makes the compilation of data originated from different researchers very difficult or even not possible.
More than 12,900 ant species, distributed in 324 genera, are known worldwide (Bolton, 2014).This fauna has strong biogeographic patterns, with different regions containing endemic and strongly related taxa that show rapid species turnover within their borders (Fisher, 2010).Their abundance and diversity reach a peak in tropical regions and decline in temperate latitudes (Fernandez & Sendoya, 2004).The Neotropical region has the greatest ant diversity and the highest level of endemism among the different biogeographic regions in the globe (Fisher, 2010), harboring 30% of all ant species currently described (Fernandez & Sendoya, 2004).Nevertheless, there are few comprehensive inventories of the Neotropical ant fauna (but see Longino & Colwell, 1997), particularly in non-forest ecosystems.
The Cerrado, one of the biodiversity hotspots worldwide (Myers et al., 2000), comprises a mosaic of vegetation types, which includes grasslands, forests, and especially savannas of variable structure that originally covered over two million square kilometers of Central Brazil.About 10,000 plant species occurs in the Cerrado region, of which approximately 40% are endemic (Ratter et al., 1997).However, this biodiversity is highly threatened by the expansion of modern agriculture.The creation of Conservation Units in this biome is urgent, since only less than 3% of the original Cerrado area is currently preserved (Klink & Machado, 2005).
One of the best known ant faunas of Cerrado is the fauna of the "Reserva Ecológica do Panga" (hereafter Panga Ecological Station), a reserve of 409 ha located in Uberlândia, Minas Gerais, Brazil.Since 2003 several studies involving the ant fauna were conducted in this reserve (Vasconcelos et al., 2008;Campos et al., 2011;Lopes & Vasconcelos, 2008;Lopes & Vasconcelos, 2011;Pacheco & Vasconcelos, 2007;Pacheco & Vasconcelos, 2012;Powell et al., 2011;Vasconcelos et al., 2009;Camarota et al., 2015).However, a complete list of the species collected in the reserve was never compiled, since each study generated its own list of species and morphospecies and the codes used to separate the morphospecies were unique for each study.The objective of this study was to integrate information derived from the various ant surveys performed at the Panga Ecological Station, in order to provide a comprehensive list of species.For this, we examined the specimens collected in each study, identifying to species level whenever possible and, when this was not possible, assigning a standardized code for each recognized morphospecies.

Material and methods
All ants listed in this study were collected at the Panga Ecological Station (PES), a 409 ha reserved owned by the University of Uberlândia (UFU) and located 30 km south of Uberlândia,Minas Gerais State,Brazil (19° 10' S,48° 24' W).The region is characterized by a tropical climate with two distinct seasons: a dry winter (from May to September) and a rainy summer (from October to April).Average annual temperature in this locality is 22.8° C and average annual rainfall is 1482 mm.Soils at the site are primarily red latosoils.Most of the reserve is covered by savannas -of which cerrado sensu stricto is the predominant -and in addition there are patches of forests and seasonally water-logged swamps.For a more detailed description of the vegetation of the study area see Cardoso et al. (2009).
The species list provided here results from a compilation of data from 10 different ant surveys performed at PES since 2003 (Table 1).All specimens collected during these studies are deposited at the Zoological Collection of the Federal University of Uberlândia (UFU), in Uberlândia, Brazil.We examined all specimens deposited at UFU´s Zoological Collection.All material identified at the morphospecies level was revised in order to unify morphospecies codes across the studies.Once this was done, we attempted to identify the specimens using taxonomic keys (Longino, 2003;Wild, 2005;Mayhé-Nunes & Brandão, 2006;Klingenberg & Brandão, 2009;Mackay & Mackay, 2010) or by sending specimens to ant taxonomists (see acknowledgments).Sampling completeness (across all studies) was determined using the Chao 2 species richness estimator, which was calculated using the default options of EstimateS 9.1.0(Colwell et al, 2012).Based on information existing on the specimens labels and/or through information in the original data sets of the various studies listed in Table 1, we determined the habitats (savanna or forest) and the foraging strata (soil or woody vegetation) of occurrence (number of times the species was recorded in all studies) for each species and morphospecies.

Results
We recorded a total of 277 ant species from 58 genera and nine subfamilies (Appendix).Using taxonomic keys or with the aid of experts we were able to name a total of 177 species (63.9% of the total).In the previous studies conducted at PES only 24 species had been formally named.Therefore, the present study adds 153 species names for the ant fauna of the reserve.The total number of species recorded so far at the reserve represents 89.2% of the expected species number to be found there according to the species richness estimator Chao 2 (310.4 species).The diversity-dominance curve (Fig 1 ) shows a high proportion of rare species (24.9% of the total), i.e. of species that were collected only once or twice.
The subfamily Myrmicinae was the most diverse, with 153 species, followed by Formicinae with 43 species and Dolichoderinae and Ponerinae, with 23 species each.The most diverse genus was Pheidole with 39 species, followed by Camponotus with 35 and Cephalotes, with 17 species.The most frequent species was Camponotus crassus Mayr, 1862, with 442 records of occurrence, followed by Cephalotes pusillus (Klug, 1824), Pheidole oxyops Forel, 1908 and Pheidoleradoszkowskii Mayr, 1884 with 348, 337 and 306 records, respectively.More species were recorded in the savanna (249 species) than in the forest habitats (108 species), and more species were collected on ground (226 species) than in the arboreal vegetation (117 species).A total of 160 species from 56 genera were only found on ground, whereas 51 species from 23 genera were only found in the woody vegetation.Regarding species occurrences in different vegetation types, 169 species were collected exclusively in the savanna habitats, 28 only in the forest habitats, and 141 in both.

Discussion
The data presented here represents one of the most intensive ant inventories conducted in the Brazilian Cerrado.We found that at least 277 ant species coexist within the 409 hectares of Panga Ecological Station.This number of species is nearly as high as the number of species recorded by Silvestre et al. (2004) in seven different Cerrado localities (333 species in total) and higher than the number of species recorded in savannas of Africa and Australia (Table 2).However, it is important to mention that the elevated number of species recorded at PES may only reflect the higher diversity of sampling methods and/or the higher intensity of sampling at this reserve compared to the other savannas areas sampled so far.
Only 66 species were recorded both on ground and in the woody vegetation, indicating that, as also observed in tropical forests (Bruhl et al., 1998;Vasconcelos & Vilhena, 2006;Wilkie et al., 2010) and in other Cerrado areas (Campos et al., 2008), there is a vertical stratification of the ant fauna.Camponotus, Pseudomyrmex and Pheidole were the most frequent genera in the vegetation, whereas Pheidole, Camponotus and Solenopsis were the most frequent ones on ground.Differences in species composition were also clear.The most abundant species in the vegetation were Camponotus crassus and Cephalotes pusilus, whereas on ground Pheidole oxyops and Pheidole radoszkowskii were the most abundant ones (Fig 2).Therefore, the high diversity of ants in the Cerrado reserve we studied can be explained, at least in part, by the specialization of some species to forage and/or nest either on ground or in the vegetation (Campos et al., 2008).Habitat specialization is probably also involved since many of the species inhabiting the savannas were not recorded in the forest habitats and vice-versa (Fig 3).Taxonomic identification was possible for 171 of the 277 species collected at PES.Although many of the named species are widely distributed in Neotropics (Fernandez & Sendoya, 2004) some are poorly known.For instance, Pheidole superba Wilson, 2003, was previously known only from its type locality in Colombiaand from Panamá (Wilson, 2003).Similarly, Crematogaster crucis Forel, 1912 and Myrmicocripta urichi Weber, 1937 were recorded for the first time in Brazil (Ant Wiki, 2014).Cyatta abscondita Sosa-Calvo, Schultz, Brandão, Klingenberg, Feitosa, Rabeling, Bacci, Lopes & Vasconcelos, 2014, the only representative of the newly described genus Cyatta, is also present at PES.The same is true for Cephalotes specularis Brandão, Feitosa, Powell & Del-Claro, 2014, a newly described species that presents a remarkable social parasitism behavior (Powell et al., 2014).In addition, Pseudomyrmex curacaensis (Forel, 1912) and Pseudomyrmex euryblemma (Forel, 1899) are recorded for the first time in the Cerrado region (Rodrigo M. Feitosa, Departamento de Zoologia da Universidade Federal do Paraná, personal communication, December 12, 2014).
Among the 106 unidentified species, at least six of them represent new, undescribed species, including five species of Trachymyrmex (Antônio Mayhé-Nunes, Departamento de Biologia Animal, Universidade Federal Rural do Rio de Janeiro, personal communication, July 2010) and one species of Xenomyrmex (Lívia P. Prado, Museu de Zoologia da Universidade de São Paulo, personal communication, February 14, 2014).Together, these results highlight the conservational potential of this Cerrado reserve.The Panga Ecological Station harbors a surprisingly high number of ant species indicating that, although poorly studied, the Cerrado has a highly diverse ant fauna.Moreover, the large number of species that remain unnamed shows that the ant fauna of this region is taxonomically poorly known, emphasizing the need for a greater effort in the collection and description of new species.
Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata.

Fig 1 .
Fig 1. Diversity-abundance curve of all ant species collected at the Panga Ecological Station.

Fig 2 .Fig 3 .
Fig 2. The most abundant ant genera (A) and most abundant species (B) collected on ground or in the woody vegetation.

Table 2 .
Number of ant species recorded in different tropical savannas areas of the world.

sampled Ant species richness Number of samples Sampling methodology Type of habitat Source
*Including manual collection, pitfall traps, subterranean pitfall traps, color trays, light traps, Malaise traps and Winkler extractors.
Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata.(Continuation).Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).Appendix.List of species recorded at the Panga Ecological Station.Numbers represent the total number of occurrences in different habitats or strata (Continuation).