Inventory, colony fluctuation, and wasp nesting social habits in IFSULDEMINAS-Machado Campus

Social wasps offer important ecosystem resources as biological control and pollination. Many species are synanthropic, however, there are still few studies of these insects in anthropized environments. The objective of this study was to verify the richness, colony fluctuation, and preferential substrates for social wasp nesting at IFSULDEMINAS Campus Machado. Four censuses/inventories were carried out from November 2015 to June 2016, and the active collection method with an entomological net was used for wasp collection. The specimens found were assembled, identified, and deposited in the collection of the entomology laboratory of the institution. In total, 20 species of social wasps were registered, from which the genera Polybia, Polistes, and Mischocyttarus showed a greater richness of species. The number of colonies increased from November to March, decreasing in June. Mischocyttarus cassununga R. von Ihering (1903) had more abundance of colonies in all months evaluated. Broadly, the genera Mischocyttarus and Polistes presented nesting preference for the building substrate, while the genus Polybia presented preference for the vegetation substrate. Machado Campus has a diversity of environments that contributes to the establishment of social wasp colonies. Therefore, it is essential to disseminate this information and environmental education actions to the community to demonstrate the importance of these insects for the ecosystem and the need for environmental conservation to guarantee their ecosystem services.


Introduction
Social wasps, popularly known as "marimbondos" or "cabas," are recognized mainly by the presence of their colony, called "caixa" or "enxu," and by their painful stings . Such insects belong to the order Hymenoptera, superfamily Vespoidea, family Vespidae and subfamily Polistinae. The Polistinae are cosmopolitan eusocial insects, however, the greatest diversity is found in tropical regions, especially in the neotropical region. This subfamily has 26 genera and 974 species. In Brazil it is represented by 22 genera and more than 300 species, 104 of which are endemic, thus characterizing one of the richest faunas of the subfamily Polistinae in the world which are considered important pests of several crops (GALLO et al., 2002). This preference for such prey was observed in several studies when analyzing foraged resources, for example, by Polistes versicolor Olivier (1791) (PREZOTO; CLEMENTE, 2010), Polybia occidentalis Olivier (1791), and Polybia paulista Von Ihering (1896) (HERDINA et al., 2016).
Even with all the importance of ecosystem services offered by social wasps, there is still little research on them in urban environments (ALVARENGA et al., 2010;JACQUES et al., 2012JACQUES et al., , 2015PIRES, 2017), even in the southeast region, which is the most studied in Brazil (SOUZA;VALE;. In this way, more studies are needed to better understand this process of association of social wasps with the urban environment, as well as for a better relationship between men and insects (LIMA; LIMA; PREZOTO, 2000;OLIVEIRA et al., 2015;FORTES et al., 2017). Therefore, the objective of this work was to inventory the species of social wasps and verify the number and fluctuation of colonies and preferential substrates used for nesting in the premises of the Federal Institute of Education, Science and Technology of Southern Minas Gerais (IFSULDEMINAS), Machado Campus.

Materials and methods
The study was conducted at IFSULDEMINAS -Campus Machado, Machado/MG. The municipality has typical vegetation of the seasonal semideciduous forest, Atlantic Forest biome (IBGE, 2012). It is characterized by both the climate of the Cwa type, humid subtropical with dry winter and hot summer (KÖPPEN, 1948) and the average annual temperature and rainfall of 21.2°C and 1,824 mm, respectively (MOURA et al., 2007). For the inventory of the social wasps, we conducted monthly collections in November 2015 and in January, March, and June 2016, totalizing four collections, with a total sampling effort of 96 hours. The active collection method was used to carry out the inventory, defining a route that was repeated monthly.
We examined, in each collection, the constructed areas in the Campus, such as buildings, light posts and garden plants, observing the presence of social wasps and accounting for all colonies along this route. The wasps found in colonies or mid-flight were collected with an entomological net and stored in containers with 70% alcohol. The colonies observed were photographed with A NIKON D3100 digital camera.
The specimens collected were pinned for identification, and are deposited in the collection of the entomology laboratory of the institution. The identification was made through entomological keys (RICHARDS, 1978;CARPENTER;MARQUES, 2001) and from the comparison with the biological collection of social wasps (CBVS) of IFSULDEMINAS -Inconfidentes Campus. The identification of the species was confirmed by Dr. Marcos Magalhães de Souza, from the same institution, and some specimens of the Mischocyttarus de Saussure (1853) were sent to Dr. Orlando Tobias Silveira from the Paraense Emílio Goeldi Museum in Belém -Pará.
The types of substrates used by the social wasps were grouped according to Lima, Lima, and Prezoto (2000) in the following categories: construction (walls, cement structures, and tiles); metal structures (air conditioning, gutters, construction iron, nails, screws, and lamp support); synthetic materials (plastics, rubbers, glasses); wood (masonry structures), and vegetation (all plants where nests were found). In addition to the substrate, the height of the colonies in relation to the soil was grouped into three categories: low (up to two meters), medium (from two to five meters) and high (more than five meters). The collected data were tabulated in spreadsheets (Calc -LibreOffice) for evaluation of the species richness, abundance, and fluctuation of the number of colonies over the months studied.

Results and discussion
In Machado Campus from November 2015 to June 2016, a total richness of 20 species of social wasps distributed in seven genera was registered. This richness represents 11.76 % of the total species registered in the Atlantic Forest, an area considered an important refuge for the conservation of these insects in Brazil . The genus Polybia Lepeletier (1836) showed greater species richness (seven), followed by Mischocyttarus de Saussure (1853) with five, Polistes Latreille (1802) with three, Agelaia Lepeletier (1836) with two, and Apoica Lepeletier (1836), Synoeca de Saussure (1852), and Brachygastra Perty (1833) with one species each. Similar results in anthropogenic environments were found by Oliveira, Souza, and Pires (2017), and Jacques et al. (2012), who registered a richness of 16 species distributed in 6 genera and 20 species in 9 genera, respectively.
We registered colonies of 16 species and, of the total colonies observed, 80.90 % belong to the genus Mischocyttarus, of which 94.15 % refer to the species M. cassununga (TABLE 1). The high abundance of this species may be related to the small size of its colonies and their low aggressiveness CASTRO et al. 2014), thus not representing a threat to human eyes, which decreases the risk of anthropogenic depredation. * It was not possible to collect individuals from these colonies, as they were in a place of difficult access. However, considering the pattern of their architecture, they could be identified at the genus level.
The second most representative genus in the number of colonies was Polystes (15.49 %) (TABLE 1). According to Prezoto et al. (2007), wasps of this genus feed on insects such as defoliating caterpillars and aphids, commonly found in gardens and crops, typical environments on Machado Campus that may be providing the abundance of colonies of this species.
The significant number of colonies in anthropogenic areas demonstrates that these sites have favorable conditions for the establishment of social wasps (FERREIRA; SINZATO, 2007). In turn, Machado Campus has a diversity of environments, such as constructions, gardens, agricultural production areas, and forest fragments. Alvarenga et al. (2010), Bueno, Souza, and Clemente (2019), and Jacques et al. (2012Jacques et al. ( , 2015 described that environmental heterogeneity, as well as the presence of green areas, are fundamental to the occurrence and abundance of social wasps. In neotropical regions, where climatic seasons are not well defined, the foundation of new colonies is asynchronous, so it can occur at any time of the year (ROCHA, 2011). During the four months of collection, a monthly average of 771.25 social wasp colonies was observed. As for the genera Mischocyttarus, Polystes and Polybia, there was an increased number of colonies from November to March, decreasing in June (TABLE 1). A greater abundance of social wasps in warmer and rainier periods was also observed by Alvarenga (2012) and . This happens because the seasonality of climatic factors influences wasp foraging activities , and the rainy season is more favorable because there is greater availability of food resources (CASTRO et al., 2014).
In addition to environmental factors, anthropic depredation directly influences the reduction in the number of larger colonies, such as the genus Polybia, because the size of the colony is related to the danger level of the species (LIMA; LIMA; PREZOTO, 2000), a fact also observed in this study . Rocha (2011) found that 60 % of the abandonment of colonies of the Polybia platycephala slyventris Richards (1978) species occurred due to anthropogenic action, especially in the period of intensification of civil works.
The chosen substrate for nesting also interferes with colony success (CASTRO et al., 2014;TORRES et al., 2014). In Machado Campus, the independent foundation genera, Mischocyttarus and Polistes, which presented the greatest abundance of colonies, had a preference for nesting on artificial substrates (constructions, metal structures, wood, and synthetic material) to the detriment of vegetation substrate (TABLE 2, FIGURE 2a-d, f-j, l, FIGURE 3), which was also was found by Lima, Lima, and Prezoto (2000). These substrates offer more protection against climatic variations when compared to herbaceous plants, and those that have small and deciduous leaves (CASTRO et al., 2014). Besides protection against weather conditions, nesting in human housing reduces interspecific competition and predation (TORRES et al., 2014).    Among the Polistes species, we observed that Polistes ferreri Saussure (1853) preferred metal structures (77 %), and most of its colonies were found near the air conditioners installed in the buildings surveyed (FIGURE 3d, e), where the wasps were spotted foraging probably by the water released by the equipment. In dry and cold seasons, this resource is a determining factor for the survival of individuals due to the decrease in food resources .
In addition to the substrate, the height of the colonies is crucial to their success, especially for those independent foundation species that have few individuals per colony (PREZOTO; CLEMENTE, 2010). In the present work all species of the genus Polistes and the Mischocyttarus cassununga R. von Ihering, (1903) species built their colonies between two and five meters from the ground (79 % and 70 %, respectively). These species have a preference for nesting in human housing, and the height of colonies is equivalent to that of windows and roofs, making them more discreet for human perception, which is possibly a strategy against depredation (ALVARENGA et al., 2010;SINZATO, 2007;ALVARENGA, 2012;CASTRO et al., 2014) (FIGURE 2 a-d,f-h,j,l). Unlike M. cassununga, colonies of the Mischocyttarus drewseni de Saussure (1954) and Mischocyttarus rotundicollis Cameron (1912) species were found preferentially in the low height category (54 % and 59 %, respectively), but were generally in more protected locations and with the lower flow of people.
Similarly to Polistes and M. cassununga, the genus Polybia presented a preference for nesting in the average height category (70 %), but the preferred substrate for nesting was in plants (TABLE 2  and f,h,i,l). Among the species, P. platycephala slyventris was found mainly in the adaxial part of the palm tree Livistona chinensis (Jack.) R. Br. ex. Mart (FIGURE 1b). This palm tree is abundant in urban gardens and it has considerable height and broad leaves, which provides shelter and protection to social wasps against adverse weather conditions (ALVARENGA et al., 2010;ALVARENGA, 2012).
Besides L. chinensis, species of the genus Polybia have also been found in other plants. Polybia bifasciata Saussure (1854)  The genus Synoeca presented only one species, Synoeca cyanea Fabricius, (1775) and all colonies were registered only in June (TABLE 1). According to Elisei et al. (2005), this species prefers foraging throughout the day under high temperatures and low humidity, typical conditions of drier seasons. Padua et al. (2017) reported that in those seasons, people tend to view colonies of social wasps more easily due to the deciduousness of the trees.
Colonies of S. cyanea were registered only in the vegetation substrate, in the shrub Y. elephantipes (FIGURE 4e, f) and trees of the family Leguminosae as Anadenanthera sp. (FIGURE 4d) and C. pluviosa. Regarding height, in the bushes, the colony was found in the low category, and upon the trees in the high category. Oliveira, Souza, and Pires (2017) also observed this species with nesting restricted to vegetation and explained that it occurs due to the type of colony. Also, nesting of S. cyanea in Anadenanthera sp. may facilitate thermal regulation of the colony during winter, since they are deciduous plants and allow more exposure to sunlight (SOUZA, 2010). Like Synoeca, the genus Apoica presented only one species, Apoica gelida Van der Vecht (1972), being found only one colony in the substrate construction at an average height category (FIGURE 4c). Species of this genus are characterized by nocturnal habits (CARPENTER; MARQUES, 2001), therefore it is more difficult to collect them during the day (JACQUES et al., 2015).
Two species of the genus Agelaia, A. vicina and Agelaia multipicta multipicta Haliday (1836) were registered. Species of this genus are characterized by nesting in soil cavities and tree trunks (SOMAVILLA; OLIVEIRA; SILVEIRA, 2012). In this study, the A. multipicta multipicta colony was found at the base of the C. pluviosa trunk (FIGURE 4a, b). Although the A. vicina colony was not found, it was the most abundant among the species captured in attractive traps in the vegetable garden of Machado Campus (FORTES; FORTES; FERNANDES, 2018).
The richness and abundance of social wasp colonies found in IFSULDEMINAS -Machado Campus show that these insects are part of the daily lives of the people. However, the occurrence of many species in anthropogenic environments is threatened due to human depredation of colonies, mainly by the indiscriminate use of insecticides CASINO, 2004). Thus, environmental education is essential to inform about the ecosystem's importance of social wasps and to promote their conservation (PÁDUA et al., 2017;OLIVEIRA et al., 2015;SOUZA, 2010).

IFSULDEMINAS -Machado
Campus has a diversity of environments that contributes to the settling of colonies of social wasps. Over the months studied, we observed a decrease in the number of colonies from the rainy to the dry season. The genus Polybia had more richness of species, but the genus Mischocyttarus, especially the species Mischocyttarus cassununga, had more abundance of colonies in all months evaluated, which owes to their preference for human-housing nesting and their low aggressiveness. Given the synthropy of social wasps, it is essential that the community, which has direct contact with the insects, knows their importance and preserve them. Therefore, environmental education actions are necessary to both disseminate such information and teach the correct management of the colonies.