Stingless bees are a highly diverse group of social bees comprising more than 500 species native to the tropical and subtropical regions of the world (Grüter, 2020a). They form perennial colonies composed of hundreds to thousands of workers that are common visitors of many flowering plants, including several crop species (Heard, 1999; Michener, 2007). Some species of stingless bees are already successfully managed in small scale, notably those from the genus Melipona that have been traditionally used for honey production in the Americas, with several other stingless bee genera used in Africa, Asia and Oceania (Cortopassi-Laurino et al., 2006; Quezada-Euán et al., 2018; Orr et al., 2021). However, despite their great potential to be used as commercial pollinators (Cruz et al., 2005; Del Sarto et al., 2005; Slaa et al., 2006; Bispo dos Santos et al., 2009; Hikawa and Miyanaga, 2009; Nunes-Silva et al., 2013; Caro et al., 2017; Silva-Neto et al., 2019; Giannini et al., 2020; Layek et al., 2021), the large scale application of stingless bee species with this purpose is not yet as developed as for example honeybees and bumblebees (Roubik, 1995; Ramírez et al., 2018; Roubik et al., 2018). This could be a direct consequence of a general lack of knowledge about their biology and natural history. It is therefore important to understand basic aspects of their biology such as foraging activity patterns, as well as their viability to be managed prior to any potential application of stingless bee populations.

Studying the foraging patterns of bees can help to not only increase the knowledge about these important providers of ecosystem services, but also to better formulate beekeeping strategies such as colony density and proximity to both natural areas and crops. Bees tend to forage nearby their hives (Basari et al., 2018), usually ranging from a few meters to about 2 km away from their natal nests (Van Nieuwstadt and Iraheta, 1996; Araujo et al., 2004; Kuhn-Neto et al., 2009; Nunes-Silva et al., 2019). In natural conditions, colonies of a single species are usually located somewhat distant from each other with densities ranging between 0.014-16 hives/ha (Eltz et al., 2002; Silva and Ramalho, 2016). However, there is usually a large number of colonies aggregated next to each other in managed populations, resulting in increased competition for resources and high levels of orientation mistakes or “drifting” when foragers return to their hives. There is a wide variation in the rates of drifting behavior between species and/or the type of environment, being generally higher in managed in contrast to natural populations. For example, in bumblebees, drifting rates vary between 2.7% in natural or semi natural conditions to 28% in greenhouses (Birmingham and Winston, 2004; Takahashi et al., 2010; Zanette et al., 2014), while in honeybees drifting ranges from 1–5% in natural populations up to 42% in apiaries (Pfeiffer and Crailsheim, 1998; Nanork et al., 2005, 2007; Chapman et al.,2009a,b,c). This behavior can have major consequences to colony health since diseases and pathogens may spread across hives via drifted workers (Bordier et al., 2017; Nolan and Delaplane, 2017). Hence, it is a crucial factor to be considered in terms of both honey production and crop pollination.

As yet, many aspects related to foraging patterns and drifting behavior remain poorly understood in stingless bees. In this study, we used state-of-the-art radio frequency identification (RFID) tags to monitor the foraging behavior of the stingless bee Melipona fasciculata over with special interest in the drifting patterns between colonies. In particular, we tested how marking the colony entrances with different geometric patterns affected the drifting behavior. In addition, we tested if the position of the colonies had an influence in terms of the direction of the drifting rates and, finally, we correlated the data collected with the RFID system with meteorological data to understand how abiotic climatic factors affected both the bees’ lifespan and drifting rates.

By reconstructing their daily foraging activity of the stingless bee M. fasciculata, we could observe that bees forage during the entire day, with the average peak activity per colony at 9:00 in the morning (Figure 2D). In contrast, studies using similar RFID technology show that both honeybees and bumblebees have their peak foraging activity at noon, even during a permanent daylight condition in the arctic circle (Stelzer and Chittka, 2010; Susanto et al., 2018). Similarly to honeybees, stingless bee workers perform different tasks along their lives, from taking care of the young and cleaning the colony soon after emerging, to carrying out more dangerous tasks such as defending the hive and foraging toward the end of their lives with some degree of specialization in certain tasks (Mateus et al., 2019). In the congeneric M. beecheii it was shown that some foragers collected mostly pollen whereas some others were specialized in foraging for nectar, with great impact both in their daily activity and lifespan. Nectar foragers were active during the entire day but died approximately 3 days after they began foraging, while pollen foragers were only active for 1–3 h in the early morning but lived on average 9 days after they started foraging (Biesmeijer and Tóth, 1998). These patterns could explain the differences observed in our experiments, where we detected a wide variation in their activity span (1.2–72.5 days). Despite the average extranidal activity span observed in our experiment being seemingly short (9.3 days), it is in line with a similar experiment performed with RFID system in honeybees in which individuals in control colonies lived on average 12.2 days after being introduced to the hives (Thompson et al., 2016). In addition, even though we did not quantify the precise age of the workers, Melipona bees usually start foraging around 25–33 days after emergence (Biesmeijer and Tóth, 1998; Mateus et al., 2019), hence we can estimate the life expectance of the bees in our experiments approximately between 25 and 105 days, which is consistent with what is found in the literature for M. fasciculata and other species of this genus (Grüter, 2020b).

For most social insects, life-threatening challenges increase when workers leave the security of their nests and start their foraging activity. Outside the nest they face an increased chance of predation, death by the elements (e.g., storms) or by exhaustion (Roubik, 1982; Visscher and Dukas, 1997; Gomes et al., 2015). Indeed, we observed some abiotic factors having strong effects on the bees’ activity, notably temperature, atmospheric pressure, and wind speed. An increase in the average daily maximum temperature by one degree during the bee’s lifespan corresponded to an increased activity span of 1.7 days. On the other hand, an increase in the minimum daily temperature had the opposite effect, decreasing the bee’s activity span by 3.3 days. A possible explanation for this observation is that while bees benefit from higher temperatures during daily foraging activity, the same was not true when they were inside their hives during the night, when the minimum temperatures were recorded. A similar pattern was observed for average maximum and minimum atmospheric pressure, where the maximum recorded values had a positive effect whereas minimum values had a negative effect on the bees’ foraging activity span. Finally, average recorded wind speed had a negative impact on their survival, likely by impairing the bee’s flight ability (Crall et al., 2017). Even though further studies are still needed to fully comprehend how climate factors affect the bees’ behavior, our results show that this species is highly susceptible to variations in climate factors with relatively small fluctuations having a significant impact in their lifespan, demonstrating that even small changes in the future climate might cause notable implications in their extranidal activities.

In terms of the drifting behavior, our results show that 64% of the tagged workers drifted to at least one foreign hive, and that some of them were recorded entering all seven foreign hives (Figure 3A). Bees use a combination of landmarks and polarized light to orient themselves in the environment, naturally experiencing some degree of error while returning to their nests (Rossel and Wehner, 1982; Kraft et al., 2011; Kheradmand and Nieh, 2019). The overall low density of nests in natural conditions likely sustain no strong selective pressure for higher accuracy. Nevertheless, high rates of drifting behavior are not uncommonly observed in apiaries (Free, 1958; Free and Spencer-Booth, 1961; Pfeiffer and Crailsheim, 1998), which is likely caused by the high density of hives next to each other, resulting in a larger proportion of orientation mistakes. This happens particularly when resources are abundant and guard bees become more permissive to the infiltration of non-nestmates in their hives (Pfeiffer and Crailsheim, 1998; Downs and Ratnieks, 2000). Although the levels of drifting behavior observed are likely mainly due to orientation mistakes, nest robbing or social parasitism cannot be completely ruled out, since we observed an increased proportion of drifting behavior after marking the colony entrances which presumably increased the bees ability to recognize their own colony (Plowright et al., 1995). In fact, worker social parasitism is well documented in both honeybees (Nanork et al., 2005, 2007; Chapman et al.,2009a,b, c) and bumblebees (Birmingham and Winston, 2004; Birmingham et al., 2004; Takahashi et al., 2009; Zanette et al., 2014), as well as in other social insect species including wasps (Oliveira et al., 2016). An alternative explanation for the increased proportion of drifting after marking the colony entrances could be linked with bees merely not recognizing their hive entrances. Nevertheless, this is unlikely since about half of the tagged bees (n = 1203) began foraging only after the experimental manipulation i.e., they had no prior interaction with the unmarked colony entrances. Whether workers indeed actively drift into foreign colonies and how they manage to avoid being detected as non-nestmates and attacked by guards still deserves further study.

An interesting outcome of our experimental design is the fact the nearly all drifting events took place horizontally, i.e., foragers drifted almost exclusively to colonies placed in the same shelf as their natal hive rather than above or below, and that hives placed in the center of the rows produced more drifters, similarly to what is observed in honeybees (Pfeiffer and Crailsheim, 1998). In contrast, drifting occurred preferentially in the vertical plane in two species of bumblebees, with colonies placed on top significantly receiving more drifter workers (Birmingham and Winston, 2004). These differences in the orientation of the drifting behavior are possibly due to particularities in nesting biology since bumblebees usually nest underground (Kells and Goulson, 2003), while honeybees and most stingless bee species built their nests in tree cavities or branches (Roubik, 2006; Hepburn et al., 2014). Therefore, honeybees and stingless bees would benefit more from higher accuracy in finding their nests in the vertical plane whereas bumblebees would have a stronger selective pressure toward accuracy in the vertical plane. Our finding demonstrates that the spatial distribution of colonies has important management implications for stingless bee populations. Furthermore, our results also suggest that other factors other than the position of the hives played a role in the rates of drifting behavior. In one hand, the average dew point temperature was observed to be positively correlated to the drifting levels, possible because most foraging activity happens in the early morning hours and a higher temperature overall could be linked with higher metabolic activity. On the other hand, factors like solar irradiation, maximum humidity and minimum daily temperatures were shown to negatively impact drifting rates. These factors are usually linked with lower foraging activity (de Figueiredo-Mecca et al., 2013), which could explain the reduced rates of drifting merely as an outcome of fewer foraging trips.

Stingless bees present great potential to be used in commercial crop pollination (Heard, 1999; Slaa et al., 2006; Giannini et al., 2020; Layek et al., 2021). Indeed, Melipona bees have been demonstrated to be efficient pollinators of many economically important fruits and vegetables (Cruz et al., 2005; Bispo dos Santos et al., 2009; Nunes-Silva et al., 2013; Caro et al., 2017; Silva-Neto et al., 2019). A recent study using the RFID technology with the stingless bee M. fasciculata showed that workers of this species can return to their nests from distances up to 10 km away from their hives (Nunes-Silva et al., 2019), suggesting that these bees could be well suited for pollination of large scale plantations as well.

Overall, this study presents data on the foraging activity and drifting patterns of the stingless bee M. fasciculata, showing the impact of the presence of hives nearby as well as several abiotic factors on both their lifespan and the rates of drifting behavior. This is an important step toward a better understanding of stingless bees’ biology, providing insights on how some factors might affect their application as pollinators in crops as well as in natural areas.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

VI-F, FC, and RJ had the original idea. FC, HA, RJ, LC, GP, and GV performed the experiments. PS provided the RFID system for the experiments. RO analyzed the data and wrote the first draft of the manuscript. All authors revised and approved the final version of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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