ORIGINAL RESEARCH

published: 04 August 2021

doi: 10.3389/fevo.2021.708178

Foraging and Drifting Patterns of the

Highly Eusocial Neotropical Stingless
Bee Melipona fasciculata Assessed
by Radio-Frequency Identification
Edited by:
Isabel Marques,
Tags
University of Lisbon, Portugal
Ricardo Caliari Oliveira 1* † , Felipe Andrés León Contrera 2† , Helder Arruda 3,4 ,
Reviewed by: Rodolfo Jaffé 4,5 , Luciano Costa 4 , Gustavo Pessin 4,6,7,8 , Giorgio Cristino Venturieri 9,10 ,
M. N. Kuperman, Paulo de Souza 11 and Vera Lúcia Imperatriz-Fonseca 4,12
Bariloche Atomic Centre (CNEA),
Argentina 1
Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Leuven, Belgium, 2 Laboratório
Jose Octavio Macias-Macias, de Biologia e Ecologia de Abelhas – Instituto de Ciências Biológicas, Universidade Federal do Pará – Rua Augusto Corrêa,
University of Guadalajara, Mexico Belém, Brazil, 3 Polytechnic School, Universidade do Vale do Rio dos Sinos, São Leopoldo, Brazil, 4 Vale Institute of
William G. Meikle, Technology – Sustainable Development, Rua Boaventura de Silva, Belém, Brazil, 5 Exponent, Bellevue, WA, United States,
Agricultural Research Service, 6
Vale Institute of Technology – Mining, Ouro Preto, Brazil, 7 Institute of Exact and Natural Sciences, Federal University of
United States Department Pará, Belém, Brazil, 8 Computing Department, Universidade Federal de Ouro Preto, Ouro Preto, Brazil, 9 Nativo Bees,
of Agriculture, United States Brisbane, QLD, Australia, 10 Embrapa Amazônia Oriental, Belém, Brazil, 11 School of Information Communication Technology,
*Correspondence: Griffith University, Gold Coast, QLD, Australia, 12 Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
Ricardo Caliari Oliveira
[email protected]
Bees play a key role in ecosystem services as the main pollinators of numerous
† These authors have contributed
equally to this work
flowering plants. Studying factors influencing their foraging behavior is relevant not only
to understand their biology, but also how populations might respond to changes in their
Specialty section: habitat and to the climate. Here, we used radio-frequency identification tags to monitor
This article was submitted to
Behavioral and Evolutionary Ecology,
the foraging behavior of the neotropical stingless bee Melipona fasciculata with special
a section of the journal interest in drifting patterns i.e., when a forager drifts into a foreign nest. In addition,
Frontiers in Ecology and Evolution
we collected meteorological data to study how abiotic factors affect bees’ activity and
Received: 11 May 2021
behavior. Our results show that only 35% of bees never drifted to another hive nearby,
Accepted: 15 July 2021
Published: 04 August 2021 and that factors such as temperature, humidity and solar irradiation affected the bees
Citation: drifting rates and/or foraging activity. Moreover, we tested whether drifting levels would
Oliveira RC, Contrera FAL, decrease after marking the nest entrances with different patterns. However, contrary to
Arruda H, Jaffé R, Costa L, Pessin G,
Venturieri GC, de Souza P and
our predictions, there was an increase in the proportion of drifting, which could indicate
Imperatriz-Fonseca VL (2021) factors other than orientation mistakes playing a role in this behavior. Overall, our results
Foraging and Drifting Patterns of the
demonstrate how managed bee populations are affected by both nearby hives and
Highly Eusocial Neotropical Stingless
Bee Melipona fasciculata Assessed climate factors, offering insights on their biology and potential commercial application
by Radio-Frequency Identification as crop pollinators.
Tags. Front. Ecol. Evol. 9:708178.
doi: 10.3389/fevo.2021.708178 Keywords: stingless bee, radio-frequency identification, Melipona fasciculata, foraging activity, drifting behavior

Frontiers in Ecology and Evolution | www.frontiersin.org 1 August 2021 | Volume 9 | Article 708178
Oliveira et al. RFID Monitoring of Melipona fasciculata

INTRODUCTION study, we used state-of-the-art radio frequency identification

(RFID) tags to monitor the foraging behavior of the stingless
Stingless bees are a highly diverse group of social bees comprising bee Melipona fasciculata over with special interest in the drifting
more than 500 species native to the tropical and subtropical patterns between colonies. In particular, we tested how marking
regions of the world (Grüter, 2020a). They form perennial the colony entrances with different geometric patterns affected
colonies composed of hundreds to thousands of workers that are the drifting behavior. In addition, we tested if the position of
common visitors of many flowering plants, including several crop the colonies had an influence in terms of the direction of the
species (Heard, 1999; Michener, 2007). Some species of stingless drifting rates and, finally, we correlated the data collected with the
bees are already successfully managed in small scale, notably RFID system with meteorological data to understand how abiotic
those from the genus Melipona that have been traditionally climatic factors affected both the bees’ lifespan and drifting rates.
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). MATERIALS AND METHODS
However, despite their great potential to be used as commercial
pollinators (Cruz et al., 2005; Del Sarto et al., 2005; Slaa et al., Study Species and Experimental Design
2006; Bispo dos Santos et al., 2009; Hikawa and Miyanaga, 2009; This study was performed with the stingless bee Melipona
Nunes-Silva et al., 2013; Caro et al., 2017; Silva-Neto et al., fasciculata, which has its natural distribution in the northern
2019; Giannini et al., 2020; Layek et al., 2021), the large scale region of Brazil (Pedro, 2014). The colonies used in the
application of stingless bee species with this purpose is not yet experiment were located at the meliponary of Eastern Amazon
as developed as for example honeybees and bumblebees (Roubik, Embrapa, in an environment consisting of a mosaic of
1995; Ramírez et al., 2018; Roubik et al., 2018). This could agricultural crops, forest remnants, and human habitations,
be a direct consequence of a general lack of knowledge about where worker bees could forage freely on their expected range
their biology and natural history. It is therefore important to of about 2.5 km (Van Nieuwstadt and Iraheta, 1996; Araujo
understand basic aspects of their biology such as foraging activity et al., 2004; Kuhn-Neto et al., 2009; Nunes-Silva et al., 2019).
patterns, as well as their viability to be managed prior to any The climate at the site is characterized as tropical with daily
potential application of stingless bee populations. mean precipitation of at least 60 mm throughout the year
Studying the foraging patterns of bees can help to not (Alvares et al., 2013).
only increase the knowledge about these important providers To analyze the foraging and drifting patterns of M. fasciculata,
of ecosystem services, but also to better formulate beekeeping eight experimental colonies were housed in identical hives
strategies such as colony density and proximity to both natural designed for stingless bees and located in a shed consisting of two
areas and crops. Bees tend to forage nearby their hives (Basari parallel rows with four colonies each that were placed 15 cm apart
et al., 2018), usually ranging from a few meters to about 2 km (Figure 1A). A plastic tube that extended the colony entrance and
away from their natal nests (Van Nieuwstadt and Iraheta, 1996; allowed the positioning of the antennae and microcomputer of
Araujo et al., 2004; Kuhn-Neto et al., 2009; Nunes-Silva et al., the RFID system was placed in the front of the hive. The entire
2019). In natural conditions, colonies of a single species are system was enclosed inside a box that protected entrance tubes
usually located somewhat distant from each other with densities from direct light in order to not disturb the forager’s behavior
ranging between 0.014-16 hives/ha (Eltz et al., 2002; Silva and (Figure 1B). Young worker bees that were not yet foraging
Ramalho, 2016). However, there is usually a large number of were randomly sampled from each hive to receive the RFID
colonies aggregated next to each other in managed populations, tags. Bees were tagged every week for 9 consecutive sessions
resulting in increased competition for resources and high levels with 40 workers tagged per week, amounting to 360 bees per
of orientation mistakes or “drifting” when foragers return to colony and 2,880 in total. The process consisted in collecting the
their hives. There is a wide variation in the rates of drifting young workers in the early morning (8:00–9:00) and placing them
behavior between species and/or the type of environment, being in a tube with maximum 5 workers per tube prior to tagging
generally higher in managed in contrast to natural populations. them with the RFIDs. The RFID-tags were then glued with
For example, in bumblebees, drifting rates vary between 2.7% cyanoacrylate adhesive onto the worker thorax (Figure 2B) and,
in natural or semi natural conditions to 28% in greenhouses after all bees were marked and the glue sufficiently dried, they
(Birmingham and Winston, 2004; Takahashi et al., 2010; Zanette were returned to their original hive. Workers from M. fasciculata
et al., 2014), while in honeybees drifting ranges from 1–5% tolerated well the RFID-tags glued on their thorax without any
in natural populations up to 42% in apiaries (Pfeiffer and apparent disturbance to their flight behavior (Nunes-Silva et al.,
Crailsheim, 1998; Nanork et al., 2005, 2007; Chapman et al., 2019; Gomes et al., 2020; Costa et al., 2021). Finally, after
2009a,b,c). This behavior can have major consequences to colony 42 days of the beginning of the experiment, colonies received
health since diseases and pathogens may spread across hives via simple geometrical individual black and white markings made
drifted workers (Bordier et al., 2017; Nolan and Delaplane, 2017). with electrical tape at their entrances to test whether foragers
Hence, it is a crucial factor to be considered in terms of both would then improve recognition of their own hive and drift to
honey production and crop pollination. fewer foreign hives, i.e., make fewer orientation mistakes. The
As yet, many aspects related to foraging patterns and drifting experiment ran for another 78 days after the marking of the
behavior remain poorly understood in stingless bees. In this colony entrances until the activity of tagged bees was no longer

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Oliveira et al. RFID Monitoring of Melipona fasciculata

Data Analysis
All statistical analyses were carried out using the R software
(R Core Team, 2020). Data filtering and merging RFID and
meteorological data was performed using a custom R script
(available on data repository). Extranidal activity span of foragers
was calculated based on the difference between the last recorded
data and the date the bees were tagged (Decourtye et al., 2011;
Tenczar et al., 2014; Perry et al., 2015; Dosselli et al., 2016;
Santoro et al., 2019). First foraging trip was calculated with the
difference between the first trip recorded and the tagging date
and the kernel density estimates were calculated based on the
smoothed histogram using the “geom_density” function in the R
package ggplot2. Likewise, the daily foraging activity were also
calculated using the density function in the package ggplot2.
To analyze the influence that both biotic and abiotic factors
have on the observed drifting rates we used a model selection
approach using the package glmulti to select the best set of
explanatory variables based on the models Akaike’s Information
FIGURE 1 | (A) Experimental setup scheme not to scale with four hives in the
Criterion. The selected best model had drifting numbers coded
top shelf and four in the bottom shelf. The RFID systems were placed in a
plastic box at the hive entrances. (B) Inside view of the entrance box as the dependent variable with activity span, hive ID, number of
containing the RFID system. 1, box containing the Intel Edison and Breakout days to begin foraging as well as several meteorological factors
Board; 2, RU-824 antenna; 3, tube connecting the hive to the entrance, and coded as covariates with a Poisson error distribution. We then
4, protective plastic casing. used the same approach to select a model with the bees’ lifespan
coded as the dependent variable but used a quasipoisson error
distribution do deal with overdispersion detected in this model.
observed. Despite the unbalanced number of days before and In addition, we tested whether the proportion of drifters present
after marking the colony entrances, the number of worker bees on the colonies was different before and after marking the colony
tracked during each period was similar (n = 1496 workers during entrances by fitting a binomial GLMM with the proportion of
control and n = 1,203 during the experimental period). foragers that drifted to an unrelated colony as the dependent
variable, colony marking (before or after) as a fixed factor and
hive ID and an observation-level random effect variable to cope
RFID-System Setup with overdispersion as random factors. Finally, we tested whether
This study was conducted using the Radio Frequency drifters had any preference on the direction they would drift. To
Identification System Ultra Small Package Tag (USPT) developed this end, we ran a binomial GLM with the direction of the drifting
by Hitachi Chemical (Endou et al., 2014). The system consisted event (i.e., horizontal and vertical) as the dependent variable,
in a single antenna placed below the colony entrance tube both the natal hives ID and the host hives ID as cofactors and
connected to an Intel Edison micro-computer to store data individual IDs as a random factor. When appropriate, models
(Figure 1B). Each tag was recorded with an individual ID were tested for temporal autocorrelation, which was not observed
that included the bee number and her colony of origin prior in the data. The R script used in the analyses as well as the original
to being glued onto the bees. Therefore, whenever a tagged datasets are publicly available in the data repository (Oliveira
bee passed through the entrance tube both worker ID and et al., 2021). All models presented in the results section are
time of the day were recorded. A caveat of the experimental Poisson GLMs unless otherwise specified. In addition, Wald Z
design was that our system consisted of only one reader per Scores are shortened to Z throughout the text.
colony, hence the signal sent to the computer did not inform
the directionality of the bee’s movement (toward or away
from the hive) which was then mitigated during data analysis. RESULTS
Moreover, guard bees staying by the colony entrance would
have repeated readings over a short period of time. Hence, Bees Extranidal Activity
only signals that were at least 180 s apart were included in Our results show that the tagged workers were active on average
the analysis to resolve this issue. Thresholds between 60 s and for 9.3 days, ranging from a minimum of 1.2 to a maximum
5 min are consistently used to filter RFID foraging data in of 72.5 days after being tagged (Figure 2A). In addition, bees
Hymenoptera (Lach et al., 2015; Dosselli et al., 2016; Susanto began foraging on average 2 days after being tagged, with
et al., 2018; Santoro et al., 2019). This threshold was adopted some more extreme cases where workers only started foraging
during data filtering in order to reflect only the extranidal flight after 25 days and beyond, as registered by the first reading of
activity. We opted for this threshold because, while it might their tags at the colony entrance (Figure 2C). Foragers were
misrepresent short patrolling flights, it prevents overestimating active throughout the day, with most activity being recorded
their foraging activity. during the early morning hours (between 5:00–10:00), reaching

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Oliveira et al. RFID Monitoring of Melipona fasciculata

FIGURE 2 | (A) Workers extranidal activity span based on the difference between the last reading on the RFID system and the day they were tagged. Different
colonies are plotted on the y axis with every row corresponding to an individual bee sorted by activity span. The vertical gray line represents the mean activity of
9.3 days. (B) Picture of a M. fasciculata forager with a RFID tag on her thorax. Photo by GV. (C) Kernel density estimate plot of the bees’ first foraging trip calculated
as the difference between the tagging data and the first record on the reader. (D) Kernel density estimate plot calculated by the overall frequency of reads per colony
per day displaying the bees’ activity throughout the day. Peak activity was recorded between 5:00 to 10:00 in all colonies.

the peak activity at 9:00 and then decreasing until 18:00 or right rather than above or below their natal hives (Binomial
(Figure 2D). Furthermore, our data show that workers in colony GLMM, Z > 8.568, p < 0.001 for all colonies, Figure 4B).
four showed significantly less activity, while in colony one and Moreover, colonies placed on both edges produced fewer drifters
two significantly more activity than the average was recorded than colonies placed between other hives. For instance, foragers
(colony four: Z = −7.602, p < 0.001; colony one: Z = 2.373, in colonies two, three, six and seven showed significantly higher
p = 0.047; colony two: Z = 5.478, p < 0.001). Figure 3 illustrates levels of drifting behavior (hive two: Z = 11.880, p < 0.001; hive
the reconstructed foraging activity of all 2,880 bees during the three: Z = 11.499, p < 0.001; hive six: Z = 4.125, p < 0.001 and
4-month study period. hive seven: Z = 3.514, p = 0.001) while hives four, five and eight
had significant fewer drifters (hive four: Z = −5.746, p < 0.001;
hive five: Z = −5.250, p < 0.001 and hive eight: Z = −9.716,
Factors Affecting Drifting Behavior and p < 0.001), with hive one being not significant (Z = 0.181,
Foraging Activity p = 0.936). Furthermore, drifting rates were positively correlated
Throughout the study period, 64.1% of all tagged workers with workers’ lifespan Z = 18.113, p < 0.001) and the sooner bees
drifted to at least one other colony, with 36.6% drifting to began foraging after being tagged the higher the observed drifting
only one, 19.1% to two, 7.6% to three foreign colonies, and rates (Z = 7.494, p < 0.001).
the percentage decreasing below 1% as the number of foreign In addition to biotic factors, several meteorological factors
colonies increased up to a maximum of seven colonies, i.e., all influenced the levels of drifting behavior, with dew point
non-natal experimental colonies (Figure 4A). It is interesting to positively affecting the drifting rates (Z = 3.205, p = 0.001),
note that the majority of the drifting events was in the horizontal while solar irradiation (Z = −2.804, p = 0.005), maximum
plane, that is, workers mostly drifted to colonies on their left relative humidity (Z = −2.883, p = 0.002) and minimum daily

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Oliveira et al. RFID Monitoring of Melipona fasciculata

FIGURE 3 | Foraging activity span of all bees during the 4-month study period. Each row represents the RFID scans of an individual bee, with the specific colors
corresponding to their respective natal hives. Therefore, bees that matched the color with their nest of origin are natal workers whereas different colors within a hive
represent the activity of foreign drifter workers. In total 2,880 bees were tagged in nine separate sessions demonstrated by the ladder-like appearance along the y
axis. That is, at every session 40 tagged bees were introduced per colony. The vertical dashed line shows when the colony entrances were marked, 42 days after
the beginning of the experiment. The experimental period ran for another 78 days until no tagged bees could be observed in the nest.

temperature (Z = −2.722, p = 0.006) were negatively correlated DISCUSSION

to the drifting rates.
During the experimental period colony entrances received By reconstructing their daily foraging activity of the stingless
individual markings to test whether foragers would then improve bee M. fasciculata, we could observe that bees forage during
recognition of their own hive and drift to fewer foreign hives, the entire day, with the average peak activity per colony at 9:00
i.e., make fewer orientation mistakes. Intriguingly, we observed in the morning (Figure 2D). In contrast, studies using similar
an increase in the proportion of drifting events after marking RFID technology show that both honeybees and bumblebees have
the hive entrances, with 63.9% of tagged bees drifting before their peak foraging activity at noon, even during a permanent
and 68.7% after the hive entrances were marked (Binomial daylight condition in the arctic circle (Stelzer and Chittka, 2010;
GLMM, Z = 2.508, p = 0.012), which could indicate factors Susanto et al., 2018). Similarly to honeybees, stingless bee workers
other than mere orientation mistakes playing a role in drifting perform different tasks along their lives, from taking care of the
behavior (Figure 4A). young and cleaning the colony soon after emerging, to carrying
Finally, it was possible to observe that meteorological factors out more dangerous tasks such as defending the hive and foraging
were also correlated with the workers extranidal activity, toward the end of their lives with some degree of specialization in
whereby maximum daily atmospheric pressure and temperature, certain tasks (Mateus et al., 2019). In the congeneric M. beecheii
precipitation as well as dew point temperature were positively it was shown that some foragers collected mostly pollen whereas
correlated with the bees activity span (max atmospheric pressure: some others were specialized in foraging for nectar, with great
Z = 6.521, p < 0.001; max temperature, Z = 5.236, p < 0.001; impact both in their daily activity and lifespan. Nectar foragers
precipitation, Z = 3.020, p = 0.002; max dew point: Z = 2.504, were active during the entire day but died approximately 3 days
p = 0.012; min dew point: (Z = 4.710, p < 0.001). Conversely, after they began foraging, while pollen foragers were only active
minimum daily temperature and atmospheric pressure, humidity for 1–3 h in the early morning but lived on average 9 days after
and wind speed negatively affecting the bees’ activity (min they started foraging (Biesmeijer and Tóth, 1998). These patterns
temperature: Z = −8.834, p < 0.001; min atmospheric could explain the differences observed in our experiments, where
pressure, Z = −6.922, p < 0.001; max humidity: Z = −4.235, we detected a wide variation in their activity span (1.2–72.5 days).
p < 0.001; min humidity: Z = −3.156, p = 0.001; and wind Despite the average extranidal activity span observed in our
speed: Z = −9.901, p < 0.001). Table 1 summarizes the experiment being seemingly short (9.3 days), it is in line with a
relationship of abiotic factors with both drifting behavior and similar experiment performed with RFID system in honeybees in
foraging activity. which individuals in control colonies lived on average 12.2 days

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Oliveira et al. RFID Monitoring of Melipona fasciculata

FIGURE 4 | (A) Percentages of drifting events to different foreign colonies during the experimental period before and after marking the colony entrances. Hives
placed in the middle sections of the shelves presented higher rates of drifting behavior with some drifters visiting all seven non-natal hives. n shows the number of
tagged worker drifters per colony per period. (B) Drifting events were mostly in the horizontal plane, with on average 96% of the drifting events being to colonies
placed on the same shelf than the natal hives.

after being introduced to the hives (Thompson et al., 2016). In chance of predation, death by the elements (e.g., storms)
addition, even though we did not quantify the precise age of the or by exhaustion (Roubik, 1982; Visscher and Dukas, 1997;
workers, Melipona bees usually start foraging around 25–33 days Gomes et al., 2015). Indeed, we observed some abiotic factors
after emergence (Biesmeijer and Tóth, 1998; Mateus et al., 2019), having strong effects on the bees’ activity, notably temperature,
hence we can estimate the life expectance of the bees in our atmospheric pressure, and wind speed. An increase in the
experiments approximately between 25 and 105 days, which is average daily maximum temperature by one degree during the
consistent with what is found in the literature for M. fasciculata bee’s lifespan corresponded to an increased activity span of
and other species of this genus (Grüter, 2020b). 1.7 days. On the other hand, an increase in the minimum
For most social insects, life-threatening challenges increase daily temperature had the opposite effect, decreasing the bee’s
when workers leave the security of their nests and start their activity span by 3.3 days. A possible explanation for this
foraging activity. Outside the nest they face an increased observation is that while bees benefit from higher temperatures

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TABLE 1 | Abiotic factors affecting both drifting behavior and foraging activity.

Drifting behavior Foraging activity

Abiotic factors Log-Mean z value p value Log-Mean t value p value

Temperature max. 1.68 5.24 < 0.001 ***

Temperature min. −0.85 −2.72 0.006 ** −3.34 −8.83 < 0.001 ***
Humidity max. −0.21 −2.88 0.004 ** −0.42 −4.23 < 0.001 ***
Humidity min. −0.27 −3.16 0.002 **
Solar irradiation instant. 0.00 −2.80 0.005 **
Dew Point instant. 0.99 3.20 0.001 **
Dew Point max. 0.99 2.50 0.012 *
Dew Point min. 1.71 4.71 < 0.001 ***
Atmospheric Pressure max. 2.73 6.52 < 0.001 ***
Atmospheric Pressure min. −2.90 −6.92 < 0.001 ***
Precipitation 0.49 3.02 0.003 **
Wind Speed −2.03 −9.90 < 0.001 ***
Wind Gust −0.16 −1.79 0.074

Estimates are presented in terms of the log mean effect size in which positive values imply a positive relationship with the dependent variable i.e., drifting behavior or
foraging activity, while negative values show a negative relationship. Only factors included in the models are shown. Significant effects are shown in bold. Significance
levels *p < 0.05, **p < 0.01, and ***p < 0.001.

during daily foraging activity, the same was not true when they since we observed an increased proportion of drifting behavior
were inside their hives during the night, when the minimum after marking the colony entrances which presumably increased
temperatures were recorded. A similar pattern was observed for the bees ability to recognize their own colony (Plowright et al.,
average maximum and minimum atmospheric pressure, where 1995). In fact, worker social parasitism is well documented in
the maximum recorded values had a positive effect whereas both honeybees (Nanork et al., 2005, 2007; Chapman et al.,
minimum values had a negative effect on the bees’ foraging 2009a,b,c) and bumblebees (Birmingham and Winston, 2004;
activity span. Finally, average recorded wind speed had a negative Birmingham et al., 2004; Takahashi et al., 2009; Zanette et al.,
impact on their survival, likely by impairing the bee’s flight 2014), as well as in other social insect species including
ability (Crall et al., 2017). Even though further studies are still wasps (Oliveira et al., 2016). An alternative explanation for
needed to fully comprehend how climate factors affect the bees’ the increased proportion of drifting after marking the colony
behavior, our results show that this species is highly susceptible entrances could be linked with bees merely not recognizing their
to variations in climate factors with relatively small fluctuations hive entrances. Nevertheless, this is unlikely since about half
having a significant impact in their lifespan, demonstrating that of the tagged bees (n = 1203) began foraging only after the
even small changes in the future climate might cause notable experimental manipulation i.e., they had no prior interaction
implications in their extranidal activities. with the unmarked colony entrances. Whether workers indeed
In terms of the drifting behavior, our results show that actively drift into foreign colonies and how they manage to avoid
64% of the tagged workers drifted to at least one foreign being detected as non-nestmates and attacked by guards still
hive, and that some of them were recorded entering all seven deserves further study.
foreign hives (Figure 3A). Bees use a combination of landmarks An interesting outcome of our experimental design is the fact
and polarized light to orient themselves in the environment, the nearly all drifting events took place horizontally, i.e., foragers
naturally experiencing some degree of error while returning drifted almost exclusively to colonies placed in the same shelf
to their nests (Rossel and Wehner, 1982; Kraft et al., 2011; as their natal hive rather than above or below, and that hives
Kheradmand and Nieh, 2019). The overall low density of nests placed in the center of the rows produced more drifters, similarly
in natural conditions likely sustain no strong selective pressure to what is observed in honeybees (Pfeiffer and Crailsheim,
for higher accuracy. Nevertheless, high rates of drifting behavior 1998). In contrast, drifting occurred preferentially in the vertical
are not uncommonly observed in apiaries (Free, 1958; Free plane in two species of bumblebees, with colonies placed on
and Spencer-Booth, 1961; Pfeiffer and Crailsheim, 1998), which top significantly receiving more drifter workers (Birmingham
is likely caused by the high density of hives next to each and Winston, 2004). These differences in the orientation of the
other, resulting in a larger proportion of orientation mistakes. drifting behavior are possibly due to particularities in nesting
This happens particularly when resources are abundant and biology since bumblebees usually nest underground (Kells and
guard bees become more permissive to the infiltration of non- Goulson, 2003), while honeybees and most stingless bee species
nestmates in their hives (Pfeiffer and Crailsheim, 1998; Downs built their nests in tree cavities or branches (Roubik, 2006;
and Ratnieks, 2000). Although the levels of drifting behavior Hepburn et al., 2014). Therefore, honeybees and stingless bees
observed are likely mainly due to orientation mistakes, nest would benefit more from higher accuracy in finding their
robbing or social parasitism cannot be completely ruled out, nests in the vertical plane whereas bumblebees would have

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Oliveira et al. RFID Monitoring of Melipona fasciculata

a stronger selective pressure toward accuracy in the vertical might affect their application as pollinators in crops as well as
plane. Our finding demonstrates that the spatial distribution of in natural areas.
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 DATA AVAILABILITY STATEMENT
the rates of drifting behavior. In one hand, the average dew
point temperature was observed to be positively correlated The original contributions presented in the study are included
to the drifting levels, possible because most foraging activity in the article/supplementary material, further inquiries can be
happens in the early morning hours and a higher temperature directed to the corresponding author/s.
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 AUTHOR CONTRIBUTIONS
impact drifting rates. These factors are usually linked with lower
foraging activity (de Figueiredo-Mecca et al., 2013), which could VI-F, FC, and RJ had the original idea. FC, HA, RJ, LC, GP, and
explain the reduced rates of drifting merely as an outcome of GV performed the experiments. PS provided the RFID system for
fewer foraging trips. the experiments. RO analyzed the data and wrote the first draft
Stingless bees present great potential to be used in commercial of the manuscript. All authors revised and approved the final
crop pollination (Heard, 1999; Slaa et al., 2006; Giannini et al., version of the manuscript.
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 FUNDING
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 This project was funded by the Brazilian National Council
with the stingless bee M. fasciculata showed that workers of this for Scientific and Technological Development CNPq, grant
species can return to their nests from distances up to 10 km 444384/2018-9; and by individual research grants to VLIF
away from their hives (Nunes-Silva et al., 2019), suggesting that (CNPq 312250/2018-5), RF (CNPq 301616/2017-5) and RCO
these bees could be well suited for pollination of large scale (Research Foundation Flanders FWO research Grant 1502119N
plantations as well. and postdoctoral Grant 12R9619N).
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 ACKNOWLEDGMENTS
factors on both their lifespan and the rates of drifting behavior.
This is an important step toward a better understanding of We would like to thank Elisângela Rêgo for helping
stingless bees’ biology, providing insights on how some factors to tag the bees.

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Res. 58, 9–15. doi: 10.1080/00218839.2018.1494913 absence of any commercial or financial relationships that could be construed as a
Slaa, E. J., Chaves, L. A. S., Malagodi-Braga, K. S., and Hofstede, F. E. (2006). potential conflict of interest.
Stingless bees in applied pollination: Practice and perspectives. Apidologie 37,
293–315. doi: 10.1051/apido:2006022 Publisher’s Note: All claims expressed in this article are solely those of the authors
Stelzer, R. J., and Chittka, L. (2010). Bumblebee foraging rhythms under the and do not necessarily represent those of their affiliated organizations, or those of
midnight sun measured with radiofrequency identification. BMC Biol. 8:93. the publisher, the editors and the reviewers. Any product that may be evaluated in
doi: 10.1186/1741-7007-8-93 this article, or claim that may be made by its manufacturer, is not guaranteed or
Susanto, F., Gillard, T., De Souza, P., Vincent, B., Budi, S., Almeida, A., et al. (2018). endorsed by the publisher.
Addressing RFID misreadings to better infer bee hive activity. IEEE Access 6,
31935–31949. doi: 10.1109/access.2018.2844181 Copyright © 2021 Oliveira, Contrera, Arruda, Jaffé, Costa, Pessin, Venturieri, de
Takahashi, J.-I., Martin, S. J., Ono, M., and Shimizu, I. (2009). Male production Souza and Imperatriz-Fonseca. This is an open-access article distributed under the
by non-natal workers in the bumblebee, Bombus deuteronymus (hymenoptera: terms of the Creative Commons Attribution License (CC BY). The use, distribution
Apidae). J. Ethol. 28, 61–66. doi: 10.1007/s10164-009-0155-y or reproduction in other forums is permitted, provided the original author(s) and
Takahashi, J.-I., Martin, S. J., Ono, M., and Shimizu, I. (2010). Male production the copyright owner(s) are credited and that the original publication in this journal
by non-natal workers in the bumblebee, Bombus deuteronymus (hymenoptera: is cited, in accordance with accepted academic practice. No use, distribution or
Apidae). J. Ethol. 28, 61–66. doi: 10.1007/s10164-009-0155-y reproduction is permitted which does not comply with these terms.

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