INTRODUCTION

Flight and foraging of social insects, such as stingless bees, are influenced both by the internal conditions of the colony and the variation of external conditions, including climatic conditions and availability of resources for foraging (^{Kleinert-Giovannini & Imperatriz-Fonseca, 1986}; ^{Kerr et al., 1996}; ^{Biesmeijer et al., 1999}; ^{Nascimento & Nascimento, 2012}).

The internal conditions of the colony are strongly influenced by the nest population that determines the amount of bees foraging (^{Kerr et al., 1996}). The body size determines the distance of flight and the response of workers to weather factors (^{Pereboom & Biesmeijer, 2003}; ^{Araújo et al., 2004}).

Environmental factors such as temperature, precipitation, light intensity, wind speed, and relative humidity influence the flight activity of stingless bees, its variation throughout the year and therefore the pollination (^{Kleinert-Giovannini & Imperatriz-Fonseca, 1986}; ^{Bruijn & Sommeijer, 1997}; ^{Hilário et al., 2003}). The flowering characteristics such as availability, time of occurrence, duration, quality and sugar concentration in nectar are also important to external activity of bees (^{Marques-Souza, 1996}; ^{Biesmeijer et al., 1999}).

Information about external activity of bees is very important because it provides data of the species biology and aspects of their behavior that impact on their potential for crop pollination (^{Iwama, 1977}; ^{Hilário et al., 2000}). These features include the amount of bees that enter and leave the hive and the resources collected by them.

Flight and foraging activity of stingless bee are better known for those species nesting in tree cavities. However, to date, few studies have addressing these issues in subterranean stingless bees. Geotrigona subterranea occurs in the Brazilian states of Bahia, Minas Gerais, Paraná and São Paulo (^{Camargo & Moure, 1996}). Its nest is built in subterranean cavities of various types, usually abandoned nests of ants and termites. The genus Geotrigona has the particularity of collecting detritus that are deposited around the entrance hole, helping the foragers in the nest location (^{Nogueira-Neto & Sakagami, 1966}; ^{Barbosa et al., 2013}). This paper aimed to evaluate the foraging pattern and harvesting of floral and non-floral resources by G. subterranea in a natural environment.

MATERIAL AND METHODS

The study was carried in the municipality of Januária, (15°29’16”S, 44°21’43”W; 554 meters of altitude), Minas Gerais, Brazil. The vegetation in the region is characterized by areas of transition between the Cerrado and Caatinga biomes. The climate type in the region, according to Köppen classification, is Aw, with a dry winter and a wet summer.

We recorded the number of bees in flight activity in two feral colonies (distanced 170 m) through the observation of the amount of bees leaving and entering the nest and the type of transported material, in order to assess the foraging strategy adopted by these bees and their adaptation to the environment. The evaluations were performed on three days per month, from 5 a.m. to 7 p.m., between December 2011 and November 2012. The amount of bees in flight activity was determined by direct counting of individuals entering and leaving the nest during the period of 10 minutes every hour for the colony, 924 observations. We calculated an average of the data for the two colonies investigated.

The type of material transported by bees was identified based on visible characteristics by each material: resin (shiny appearance); pollen (clearest colorations); and detritus (loaded in the mandibles). We also observed bees entering the colony without apparent material (WAM), presumably nectar and water (^{Roubik, 1989}).

Temperature and humidity data were taken locally using a station TFA® installed on the nests observation site. The monthly precipitation during the study period was obtained in the database of conventional meteorological stations INMET (government institution that provides information about the weather and the climate throughout Brazil).

We performed a Spearman test in order to evaluate whether there would be correlation between foraging activity of bees and climatic variables. This analysis was carried out using the Statistical Analysis System (^{SAS, 2002}).

RESULTS

Regarding external activity during the day, the bees leave the colonies after 6 a.m., seldom occurring activity prior to this time. The flight activity lasted until the interval 6-7 p.m. and after that rarely flight activities were observed (Fig. 1). Monthly flight activity and collected resources by G. subterranea varied throughout the year, occurring greater activity in May 2012, after the rainy period. In November there was the slightest movement of bees leaving and entering the colony. This was also the wettest month during the study period (Fig. 2).

Figure 1: Daily pattern of flight activity (means of 12 months and 2 nests) of workers of Geotrigona subterranea at Januária, MG, southeastern Brazil. 

Figure 2: Monthly flow of entries and exits of Geotrigona subterranea in the nests. 

The beginning of flight activity occurred at an average temperature of 19.6°C and relative humidity of 77.4% (at 6-7 a.m.), with the peak activity occurring in the range of 1-2 p.m., at an average temperature 32.5°C and humidity of 42.4%. The temperature and humidity at the end of the activity were 28.8°C and 49.7%, respectively (Fig. 3). There was a positive correlation between temperature and entering (p < 0.01) and leaving (p < 0.05) of bees. Humidity and ‘entrance in the colony’ were negatively correlated (p < 0.05), however there was no significant correlation between relative humidity and ‘leave the colony’ (Table 1).

Figure 3: Temperature and humidity range in Januária, MG, throughout the day. 

Bee’s entries in the colony WAM, presumably nectar and water, occurred throughout the day and was greater in the afternoon, reaching peak activity in the interval of 1-2 p.m. (Fig. 4). The movement of bees WAM occurred throughout the year.

Figure 4: Geotrigona subterranea flow throughout the day according to the type of transported material. 

There was pollen collection during the entire period of activity, occurring greater foraging in the interval of 11 a.m. - noon. This activity was higher in May and September (Fig. 5), during which the precipitation was 25.7 mm.

Figure 5: Monthly flow of Geotrigona subterranea according to the type of transported material. 

The gathering of resin started a little later and focused on the afternoon shift, reaching a peak between 1-2 p.m. The resin collection activity occurred in all months, although it was higher in the dry season, between the months of March and October. This activity was positively correlated with temperature (p < 0.001).

Detritus was collected from the ground, in places where there is the availability of small kindling and little pieces of leaves, petals of little flowers and small clay pellets. The collection began around 11 a.m., achieved greatest activity in the period of 2-3 p.m. and continued until 6 p.m. The bees collected detritus throughout almost the entire year, except for the months of February, June and July, with a higher activity in March (Fig. 5). The transport of detritus showed positive correlation with temperature (p < 0.001) and negative correlation with humidity (p < 0.001).

DISCUSSION

The foraging activity of subterranean stingless bees seem indeed to be affected by climatic factors. For example, the sister species G. mombuca also has been observed to be affected by temperature and relative humidity (^{Gobatto & Knoll, 2013}). Most likely both subterranean stingless bee species (G. mombuca and G. subterranea) possess similar foraging pattern not only because they are taxonomically closely related each other, but because their populations inhabit similar natural environments.

Flight activity at high temperatures can be influenced by the color and body size. Black bees, such as the species of this study, can present problems related to dehydration and individual thermal regulation (^{Pereboom & Biesmeijer, 2003}). In G. subterranea the period of maximum activity coincides with the high temperature time during the day. Despite having black color, this species is small (5.80 mm long (^{Camargo & Moure, 1996})), an important feature, since smaller Meliponini species suffer less restrictions at warmer periods, compared to larger species (^{Roubik, 1993}).

The activity of bees without apparent material (WAM) was higher during the early afternoon and this behavior can be explained by the possibility of nectar quality increment in the hottest time, since throughout the day the concentration of sugar may increase in some blossoms (^{Roubik, 1989}).

The pollen collection activity by G. subterranea was highest in the late morning, suggesting that there may be temporal partition with other bee species since most of the pollen is available in the morning (^{Roubik, 1989}) and the larger species of stingless bees tend to concentrate the pollen gathering in the first hours of the day (^{Silva et al., 2011}). This aspect can be seen in flight activity studies of relatively large species of Melipona, as M. quadrifasciata (^{Guibu & Imperatriz Fonseca, 1984}), M. bicolor bicolor (^{Hilário et al., 2000}), M. scutellaris (^{Pierrot & Schindwein, 2003}; ^{Silva et al., 2011}), M. rufiventris (^{Fidalgo & Kleinert, 2007}), M. eburnea (^{Nates-Parra & Rodriguez, 2011}). However other small species of stingless bees, including smaller Melipona presented other pattern of foraging, it is the case of M. marginata (^{Kleinert-Giovannini & Imperatriz-Fonseca, 1986}; ^{Von B Borges & Blochtein, 2005}), M. asilvai (^{Souza et al., 2006}), Geotrigona mombuca (^{Gobatto & Knoll, 2013}), Paratrigona subnuda (^{Mouga, 1984}). It is possible that smaller species of Meliponini use floral resources after they have been exploited by larger bees (^{Silva et al., 2011}).

Regarding collection of resin, the highest activity during the dry period can be explained by increased demand of this material in this period for the construction of structures in the nest, since the flow of foragers with pollen and WAM was also higher, indicating growth of the nest. The collection in the hottest hours of the day can be explained by the ease handling of the resin by bees under high temperature conditions.

The collection of detritus is intensified during periods of rain and a possible explanation for this behavior is that bees make use of this material as mulch to prevent seed germination around the entrance hole (^{Barbosa et al., 2013}). Another hypothesis is that there is a greater availability of detritus in the dry season when there is leaf fall. The occurrence of this activity only during the afternoon can be explained by the low moisture of the material in the hottest time, allowing that detritus to be more easily transported. ^{Costa-Pereira (2014}) found that two species of Melipona collect clay with less moisture to reduce the energy cost during transport.

A higher flight activity in the dry season can be explained by variations in the quantity and quality of food between different seasons (^{Roubik, 1989}). The variation in the activity influenced by climatic factors may be different depending on the season, as reported by ^{Nascimento & Nascimento (2012}) for Melipona asilvae. This difference was observed in Trigona carbonaria by ^{Heard & Hendrikz 1993}, which presented different pattern of activity between warm and cold months. ^{Vossler et al. (2010}) found that the Geotrigona argentina accumulates large amounts of nectar and pollen during the dry season and decreases the collection activity during the rainy season. Studying the flight activity of a subterranean bee species, ^{Nagamitsu & Inoue (2002}) suggested that in the collection of pollen and nectar, the response of foragers is more closely linked to variations of resources in time scale than the general availability of sources for foraging.

CONCLUSION

Even though G. subterranea makes their nests in underground, their foraging activities are very similar to others stingless bee species that usually nest on tree cavities or aerial places. This indicate that despite their particular nesting way the external factors as climatic ones (temperature, humidity, precipitation) will significantly modulate their foraging pattern in a daily and seasonal way.