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As a specialist in studies in world culture, I am pleased to report that significant scientific research is being conducted on the contributions of stingless bees to help alleviate world hunger, as is indicated in the following scientific research article which was published less than two years ago:

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ORIGINAL RESEARCH article

Front. Plant Sci., 06 May 2020 | https://doi.org/10.3389/fpls.2020.00516

A Comparative Study of Food Source Selection in Stingless Bees and Honeybees: Scent Marks, Location, or Color

📷Sebastian Koethe1, 📷Vivian Fischbach1, 📷Sarah Banysch1, 📷Lara Reinartz1, 📷Michael Hrncir2,3 and 📷Klaus Lunau1*

• 1Institute of Sensory Ecology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
• 2Departamento de Biociências, Universidade Federal Rural do Semi-Árido, Mossoró, Brazil
• 3Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil

In social bees, the choice of food sources is based on several factors, including scent marks, color, and location of flowers. Here, we used similar setups, in which two stingless bee species, Melipona subnitida and Plebeia flavocincta, and the Western honeybee, Apis mellifera, were tested regarding the importance of chemical cues, color cues, and location-dependent cues for foraging behavior. It was determined whether workers chose food sources according to (1) scent marks deposited by conspecifics, (2) the color hue of a food source, (3) the trained location or the proximity of a food source to the hive. All three species preferred the scent-marked over an unmarked feeder that was presented simultaneously, but M. subnitida showed a weaker preference compared to the other species. When trained to blue feeders all three bee species preferred blue, but A. mellifera showed the strongest fidelity. The training to yellow feeders led to less distinct color choices. Only workers of M. subnitida mostly orientated at the training position and the close proximity to the nest. Whether the distance of a feeding site influenced the choice was dependent on the tested parameter (color or scent marks) and the species. Workers of M. subnitida preferably visited the feeder closer to the nest during the scent mark trials, but choose randomly when tested for color learning. Worker honeybees preferred the closer feeding site if trained to yellow, but not if trained to blue, and preferred the more distant feeder during the scent mark trials. Workers of P. flavocincta preferred the closer feeder if trained to blue or yellow, and preferred the more distant feeder during the scent mark trials. The disparity among the species corresponds to differences in body size. Smaller bees are known for reduced visual capabilities and might rely less on visual parameters of the target such as color hue, saturation, or brightness but use scent cues instead. Moreover, the dim-light conditions in forest habitats might reduce the reliability of visual orientation as compared to olfactory orientation. Honeybees showed the most pronounced orientation at floral color cues.

Introduction

Foraging bees use visual and olfactory cues to find and select food sources and deploy innate or learned preferences to detect flowers (Lunau and Maier, 1995; Dyer et al., 2016). Primarily, a forager’s choice is biased by innate preferences for particular colors, shapes, and odors (Menzel, 1967; Giurfa et al., 1995; Lehrer et al., 1995; Lunau et al., 1996; Gumbert, 2000; Biesmeijer and Slaa, 2004; Raine and Chittka, 2007; Howard et al., 2019). These innate preferences differ among species. In several experiments, preferences for specific hues and saturation of colors could be found for honeybees and bumble bees (Lunau, 1990; Giurfa et al., 1995; Lunau et al., 1996; Papiorek et al., 2013; Rohde et al., 2013), while stingless bees sparsely show preferences for color hue or saturation (Spaethe et al., 2014; Dyer et al., 2016; Koethe et al., 2016, 2018).

With increasing foraging experience, initial individual preferences may be either consolidated or modified through associative learning (Gumbert, 2000; Sánchez et al., 2008; Roselino et al., 2016). For instance, species-specific chemical footprints deposited by bees while landing on and manipulating flowers indicate the recent presence of a forager to subsequent visitors (Hrncir et al., 2004; Jarau et al., 2004; Eltz, 2006; Saleh and Chittka, 2006; Witjes et al., 2011). An initial attraction toward the familiar scent of conspecifics (Schmidt et al., 2005) may be reinforced when individuals learn to associate the footprints with high reward levels or reversed when scent marks indicate depleted flowers (Saleh and Chittka, 2006; Roselino et al., 2016).

Learning and memory play a major role in bee foraging, enabling the repeated visit to sustainable food sources (Breed et al., 2002; Reinhard et al., 2004, 2006; Jesus et al., 2014), flower constancy (Free, 1963; Biesmeijer and Toth, 1998; Slaa et al., 1998, 2003), and the discovery of new patches of known food plants (Biesmeijer and Slaa, 2004). In addition to memorizing scent and location of resources (Reinhard et al., 2004, 2006), bees learn both color and position of landmarks, which facilitates the orientation toward food sources and the nest (Cartwright and Collett, 1983; Cheng et al., 1986, 1987; Chittka et al., 1995; Menzel et al., 2005). However, species differ concerning their learning ability (Pessotti and Lé’Sénéchal, 1981; Mc Cabe et al., 2007), which might be associated with differences in life-history and ecological traits among bee species, such as longevity of individuals (Ackerman and Montalvo, 1985), the degree of floral specialization (Cane and Snipes, 2006), and food niche-breath (Biesmeijer and Slaa, 2006).

In eusocial bees, including the stingless bees (Meliponini), bumble bees (Bombini), and honeybees (Apini), food source selection is not only based on individual foraging preferences, but relies to a large extent on social information. On their return to the nest, foragers transmit olfactory and gustatory information about the exploited food source to nestmates, which biases the subsequent food choice of the receivers (Farina et al., 2005, 2007; Mc Cabe and Farina, 2009). Moreover, returning foragers of many species announce the existence of lucrative food sources through thoracic vibrations (stingless bees: Lindauer and Kerr, 1958; Esch et al., 1965; Barth et al., 2008; Hrncir and Barth, 2014; honeybees: Esch, 1961; Waddington and Kirchner, 1992; Hrncir et al., 2011). Inactive individuals may use these mechanical signals for their decision of whether to engage in foraging or to remain in the nest. In addition, foragers of some eusocial bee species guide the recruits to the location of the exploited food patch. Honeybees (all species) use an elaborated dance language (waggle dance) communicating information about distance, direction, and quality of foraging sites (Von Frisch, 1967; Dyer, 2002). Stingless bees (few species), in contrast, lay polarized trails of species-specific pheromone marks that guide recruits with high precision toward the goal (Lindauer and Kerr, 1958; Schmidt et al., 2003; Nieh et al., 2004; Barth et al., 2008; Jarau, 2009). At the food patch, foraging choices are influenced by field-based social information, like olfactory footprints and the visual presence of con- or heterospecific foragers (Slaa et al., 2003). Depending on the composition of the foraging community at the food patch, these passively provided cues may cause local enhancement or local inhibition (Slaa and Hughes, 2009). Thus, food source selection in eusocial species is based on a complex interplay between individual preferences and social information.

Differences among social bee species regarding ecological (habitat, food niche), physiological (learning ability, visual capacity, color vision), and behavioral features (innate preferences, foraging strategy, recruitment mechanism) may result in differences concerning the parameters used in foraging decisions. With more than 500 described species, stingless bees (Meliponini) are the most speciose group of eusocial bees with very diverse characteristics regarding body size, colony size, nesting biology, brood cell arrangement, queen production, foraging strategies, and recruitment mechanisms (Michener, 1974, 2013; Johnson, 1983; Wille, 1983; Engels and Imperatriz-Fonseca, 1990; Roubik, 2006; Barth et al., 2008). Given this biological diversity, we can expect differences concerning the mechanisms of food source selection among species. In the present study, we investigated the food source selection by two stingless bee species, Melipona subnitida and Plebeia flavocincta, and the Western honeybee, Apis mellifera. Since stingless bees show only weak preferences for colors compared to other bee species (Dyer et al., 2016; Koethe et al., 2016, 2018), alternative parameters could be of importance for foraging choices. Of interest were the roles of scent marks (olfactory footprints), the color, and the location of a food source. Melipona species are known to mark food sources with olfactory footprints (Jarau, 2009; Roselino et al., 2016). For P. flavocincta, no specific information concerning scent communication is available so far (Aguilar et al., 2005). However, given that all bee species studied to this moment deposit chemical footprints at food sources (Goulson et al., 1998; Eltz, 2006; Yokoi et al., 2007; Jarau, 2009; Witjes et al., 2011), scent cues can also be postulated for this meliponine species. A. mellifera is known for marking food sources directly (Giurfa and Nunez, 1992).

The aim was to analyze how the three investigated social bee species use the parameters color, scent marks, or location differently during the colony foraging processes. We test the hypothesis that these bees possess a hierarchy in the use of the parameters color, scent marks, and location of flowers. We expect honeybees to rely more on color cues than the two stingless bee species. For the two stingless bee species, we assume that they follow scent markings of conspecifics more reliable than honeybees. Since small stingless bee might exploit nectarrich flowers by repeated visits to the same individual flower, we assume that the location of the flower is of higher importance in the smaller bees.

Materials and Methods

This study is part of a research project on color preferences in stingless bees conducted in Australia and Brazil (Köthe, 2019).

Study Site and Bee Species

The foraging behavior of the stingless bee species was investigated at the Brazilian Federal University at Mossoró (Universidade Federal Rural do Semi-Árido), located in the Brazilian tropical dry forest, the Caatinga at 5°12′13.3″S 37°19′44.8″W. For our experiments, we used two stingless bee species native to the study region, M. subnitida (six colonies) and P. flavocincta (one colony) (Zanella, 2000; Imperatriz-Fonseca et al., 2017). P. flavocincta is the smallest bee with less than 5 mm body length (Cockerell, 1912), M. subnitida is intermediate with 7.5–8.5 mm (Schwarz, 1932), and A. mellifera is the largest with more than 11 mm (Amiet and Krebs, 2012). Colonies of the stingless bee species were kept in wooden nest-boxes at the university’s meliponary (Meliponário Imperatriz) and were freely foraging. The foraging behavior of the Western honeybee, A. mellifera, was studied at the botanical garden of the Heinrich Heine University Düsseldorf, Germany at 51°11′10.7″N 6°48′14.1″E. Foragers of five nests were trained to participate in the experiment. The colony size of the three tested species differs and ranges from several thousand individuals (20.000–80.000) in a single colony of A. mellifera to several hundred (up to 1000) in M. subnitida (Wilson, 1971; Michener, 1974). For P. flavocincta, colony size has not been determined yet, but in other Plebeia species, colony size has been shown to range from 2.000 to 3.000 individuals (Roldão-Sbordoni et al., 2018).

The reasons for conducting the study on stingless bees and honeybees at different study sites were as follows: Most experimental research in Western honeybees has been done in Europe and Australia, excluding the Africanized honeybees available in Mossoro. Moreover, A. mellifera is not native in South America. Thus, direct comparison with literature data is easier when working with European Western honeybees, although direct comparison of foraging strategies in stingless bees and honeybees in the same habitat might also yield interesting results (Roubik and Buchmann, 1984). The origin of the Western honeybee is in the Middle East or Africa (Han et al., 2012) and Western honeybees have developed adaptations to get along with temperate climates (Han et al., 2012).

Bee Training

For all tests and bee species, the training was identical. Workers of all three species were trained to mass feeders offering sugar solution (50%) affixed to tripods. The training to the mass feeders started at the respective nest’s entrance. After more than 10 workers regularly foraged at the feeder, it was moved in short steps (∼1 m) away from the nest until a distance of 15 m (site 1) or 17 m (site 2) was reached. Once at the final feeding site, the mass feeder was replaced by a colored gravity feeder (10 cm diameter, 5 cm height) that was used during the experiment. The gravity feeders were either blue (edding permanent spray RAL5010 enzianblau, edding International GmbH, Ahrensburg, Germany) or yellow (only for the color test; edding permanent spray RAL 1037 sonnengelb, edding International GmbH, Ahrensburg, Germany). The colors were measured using spectrometer analysis (USB4000 miniature fiber optic spectrometer, Ocean Optics GmbH, Ostfildern, Germany) at an angle of 45° using a UV-NIR deuterium halogen lamp (DH-2000-BAL, Ocean Optics GmbH), which was connected to the spectrometer by a UV–VIS fiber optic cable (Ø 600 μm, QR600-7-UV 125 BX, Ocean Optics GmbH). To calibrate the spectrometer, a black standard (black PTFE powder, Spectralon diffuse reflectance standard SRS-02-010, reflectance factor of 2.00%, Labsphere, Inc., North Sutton, NH, United States) and a white standard (white PTFE powder, Spectralon diffuse reflectance standard SRS99-010, reflectance factor of 99.00%, Labsphere, Inc., North Sutton, NH, United States) were used (Supplementary Figure S1). After the workers accepted the colored gravity feeder (henceforth “feeder”), a training period of 30 min started, in which the bees were allowed to forage ad libitum (approximate number of foragers during training phase: M. subnitida ≈ 10 individuals; P. flavocincta ≈ 30–50 individuals, A. mellifera ≈ 30–50 individuals). Workers were not marked during the training to keep the disturbance at the feeder to a minimum. Hence, no discrimination between experienced and inexperienced workers was possible.

Experiments

Testing the Impact of Scent Marks

We conducted experiments investigating the influence of scent marks deposited at the training feeder on the choice behavior of foragers. For this experimental series, we used only blue-colored feeders. In total, we performed three trials with each bee species. In preliminary studies, this approach turned out to be most reasonable for comparative studies between these bee species. Each trial consisted of three sets of a 30-min training phase and a subsequent 5-min test phase, switching the feeder positions in pseudo-randomized order (SM1–SM3; Supplementary Table S1). After the training phase, we offered the incoming bees both the training feeder (scent-marked) and a clean blue-colored feeder (unmarked), one at each feeding site (Supplementary Table S1). During this test phase, both feeders contained sugar solution (50%). In total, we performed three trials of this experimental series with each bee species. A trial consisted of three pairs of a 30-min training phase and a 5-min test phase intermitted by 30-min training phases (SM1–SM32; Supplementary Table S1), switching the feeder positions in pseudo-randomized order. The three different bee species (A. mellifera, M. subnitida, and P. flavocincta) were tested separately. Workers that visited the feeder were either marked with nail polish on their first visit (A. mellifera and M. subnitida) or caught after landing (P. flavocincta) and released at the end of the respective 5-min test phase. Workers were allowed to participate in all three trials. To avoid pseudo-replication (A. mellifera, M. subnitida), only the first landing of an individual in each test phase was considered for the analysis. During the third test, all foragers were captured and killed by freezing to avoid pseudo-replication.

Testing the Impact of Color

In the second experimental series, we investigated the impact of color on the choice of food sites by workers. In this experimental series, we performed two different trial series with each bee species. Each trial consisted of two sets of a 30-min training phase and a subsequent 5-min test phase, switching the feeder positions in pseudo-randomized order (Supplementary Table S1). After the training phase (training feeder either blue or yellow; Supplementary Table S1), the training feeder was removed, and we offered the incoming bees a blue- and a yellow-colored feeder during the test phase, one at each feeding site (Supplementary Table S1). In trial series 1 (C1–C4; Supplementary Table S1), bees were trained to blue feeders in the first three training phases and a yellow feeder in the fourth (training to blue, retraining to yellow). In trial series 2 (C5–C8; Supplementary Table S1), foragers were trained to yellow feeders during three training phases and a blue feeder in the last training phase (training to yellow, retraining to blue). For the test phases, we used alcohol-cleaned feeders to eliminate the influence by any potential scent marks. During the test phase, both feeders offered sugar solution (50% weight on weight). Each trial series was repeated three to five times with different individuals. The bee species (A. mellifera, M. subnitida, and P. flavocincta) were tested separately and workers that visited the feeder were either marked with nail polish (A. mellifera and M. subnitida) or caught after landing on a feeder (P. flavocincta) and released at the end of the respective 5-min test phase. To avoid pseudo-replication (A. mellifera, M. subnitida), only the first landing of an individual in each test was considered for the analysis. During the fourth test, all workers were captured and killed by freezing.

Testing the Impact of Location

To test whether bees visited the feeding site closer to the nest (site 1, 15 m) more often than the farther feeding site (site 2, 17 m) the results of all above described tests (scent marks and color) were analyzed concerning the influence of distance.

Statistics

The statistical program R was used to analyze the data (R Development Core Team, 2019). The data were analyzed by testing the bees’ choices (the first decision of each test) for the different parameters (scent marks, color, distance) using a generalized linear mixed model (GLMM). We used the “lme4” package of R to analyze choices of the bees, which were assessed using GLMM with Poisson distribution of data (Bates et al., 2009; R Development Core Team, 2019). We analyzed the number of choices for each test as fixed effect and the position of the stimuli were used as random effect of the model when testing the influence of color and scent marks, while these parameters were used as random effect when testing the impact of distance on the bees’ choice behavior.

Results

In the first experimental series (influence of scent marks), foragers of all three bee species significantly preferred the previously visited training feeder over the clean feeder (Figure 1; M. subnitida: n = 239, z-value = −8.346, p < 0.001; P. flavocincta: n = 355, z-value = −12.15, p < 0.001; A. mellifera: n = 303, z-value = −10.46, p < 0.001).

FIGURE 1

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Figure 1. Landings of workers on a scent-marked and an unmarked feeder. A generalized linear mixed model was used for statistical analysis (∗∗∗p < 0.001).

In the second experimental series, we investigated the influence of color on the feeder choice by the three bee species. After training to a blue-colored feeder, all three species significantly preferred the blue feeder over the yellow feeder (Figure 2A; M. subnitida: n = 250, z-value = −10.24, p < 0.001; P. flavocincta: n = 230, z-value = −8.821, p < 0.001; A. mellifera: n = 538, z-value = −10.85, p < 0.001). When these workers were retrained to forage on a yellow feeder during the last training phase, the two stingless bee species significantly preferred the yellow feeder while honeybee workers visited both colors equally (Figure 2B; M. subnitida: n = 124, z-value = 2.667, p = 0.007; P. flavocincta: n = 71, z-value = 3.756, p < 0.001; A. mellifera: n = 278, z-value = 0.6, p = 0.549). When workers were initially trained to a yellow-colored feeder, both stingless bee species preferred the yellow feeder significantly over the blue feeder during the test, while A. mellifera preferred the blue feeder (Figure 2C; M. subnitida: n = 199, z-value = 3.318 p < 0.001; P. flavocincta: n = 303, z-value = 3.141, p = 0.002; A. mellifera: n = 556, z-value = 5.863, p < 0.001). Retraining to a blue feeder in the last training phase lead to a significant preference of the blue colored feeder in all three species (Figure 2D; M. subnitida: n = 52, z-value = −2.95, p = 0.003; P. flavocincta: n = 61, z-value = −2.632, p = 0.008; A. mellifera: n = 213, z-value = −6.74, p < 0.001).

FIGURE 2

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Figure 2. Color choices after training sessions. The three tested bee species were trained to forage on either a blue feeder (A) or a yellow feeder (C). Furthermore, the workers were retrained to the opposite color (B,D). A generalized linear mixed model was used for statistical analysis (∗∗p < 0.01; ∗∗∗p < 0.001; ns = not significant p > 0.05).

When analyzing the influence of the feeders’ positions on the food source choice, we observed that M. subnitida visited the feeding site closer to the nest during the scent mark trials (site 1, 15 m) significantly more often than the farther site (site 2, 17 m) (Figure 3; n = 239, z-value = −8.467, p < 0.001), while choosing randomly when tested for color differences (Figure 3; blue: n = 250, z-value = −0.045, p = 0.964; yellow: n = 199, z-value = 1.502, p = 0.133). Workers of A. mellifera significantly preferred the closer feeding site when they were trained to yellow (Figure 3; n = 556, z-value = −6.147, p < 0.001), but did not distinguish between the two sites when trained for blue (Figure 3; blue: n = 538, z-value = −0.951, p = 0.342; scent marks: n = 199, z-value = −1.502, p = 0.133). In the trial concerning scent marks workers of A. mellifera significantly preferred the farther away feeding site (Figure 3; n = 303, z-value = −10.46, p < 0.001). Workers of P. flavocincta preferred the closer feeding site when trained to blue or yellow (Figure 3; blue: n = 230, z-value = −5.036, p < 0.001; yellow: n = 71, z-value = −4.856, p < 0.001) and significantly visited the farther site when tested concerning scent marks (Figure 3; n = 355, z-value = −2.548, p = 0.011).

FIGURE 3

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Figure 3. Landings of workers depending on the feeding site. The number of landings at the feeding sites with 15 m (site 1, black) and 17 m (site 2, white) distance to the hive were compared for A. mellifera, M. subnitida, and P. flavocincta for the two color trials, blue and yellow, and the scent mark trial (generalized linear mixed model *p < 0.05; ***p < 0.001; ns = not significant p > 0.05).

Discussion

The results of this study show that the response to the color of feeder, scent marks, and locations differs among the tested species P. flavocincta, M. subnitida, and A. mellifera. Our results confirm previous findings about the important role of color for food plant detection in honeybees and add further findings to the diverse and sometimes less important role of color for food plant detection in stingless bees. In previous studies of color preferences in stingless bees, the results varied among species. While three species of the genus Melipona chose colors poorly, Tetragonula carbonaria chose colors according to their hue and Partamona helleri showed similar color choices as A. mellifera preferring spectrally purer colors and bluish color hues (Rohde et al., 2013; Dyer et al., 2016; Koethe et al., 2016, 2018). Particularly for the honeybee, it has been shown that besides innate preferences, absolute or differential conditioning and behavioral plasticity play important roles in how they exploit color information (Reser et al., 2012), and that strong color preferences impede learning of other features (Morawetz et al., 2013).

Workers of A. mellifera orientated most strongly according to colors. The blue-colored feeder was preferred in all tests with exception of the retraining to yellow, where A. mellifera showed no depicted choice for one of the two colors and the two stingless bee species preferred the yellow feeder. This is in accordance to previous studies showing that A. mellifera prefers blue colors over other color hues (Giurfa et al., 1995; Horridge, 2007). The two stingless bee species chose feeders according to their colors but rather preferred the feeder color of the previous training. Only when initially trained to yellow they showed weak (M. subnitida) or no preferences for the trained color (P. flavocincta). This preference for blue is in accordance with previous results of stingless bees, but also suggests that it is weaker in stingless bees than in honeybees (Dyer et al., 2016; Koethe et al., 2016). An explanation for less visually driven behavior in stingless bees could be the size differences compared to honeybees. P. flavocincta reaches a body size of 3.6–4.1 mm, M. subnitida of 7.5 mm, and A. mellifera is the largest of the three species with 13–16 mm (Hrncir and Maia-Silva, 2013; Maia-Silva et al., 2015; Imperatriz-Fonseca et al., 2017). Especially the size of the eyes, which is associated with body size, can impact the visual capacities of bees (Streinzer et al., 2016). Workers of P. flavocincta are rather small; consequently, their eyes are also small leading to poorer visual capabilities.

Both stingless bees and honeybees use scent cues to evaluate reward availability of food resources (Nunez, 1967; Butler et al., 1969; Ferguson and Free, 1979; Free and Williams, 1983; Corbet et al., 1984; Giurfa and Nunez, 1992; Giurfa, 1993; Stout et al., 1998; Williams, 1998; Stout and Goulson, 2001). In this study, all three species showed preferences for the marked feeder over the unmarked one. P. flavocincta and A. mellifera chose the marked feeder consistently (∼88% of choices), while M. subnitida preferred the marked feeder, but visited it less frequently (∼64% of choices).

Plebeia flavocincta was the only species that significantly preferred the closer feeding site when tested concerning colors and the farther feeding site when tested regarding scent marks. One interpretation is that P. flavocincta does not differentiate between colors and choses the closer feeding site, while the preference during the scent mark trial could be based on the fact that the scent marked feeder was positioned twice at the farther site and only once at the closer site. In contrast, M. subnitida was the only species in the scent mark trials that visited the food site with shorter distance to the hive more frequently. It seems likely that M. subnitida orientates on location rather than on scent marks. Previous studies showed that species of the genus Melipona mark food sites directly and do not lay scent trails (Hrncir et al., 2004). In order to recruit new foragers, it seems possible that M. subnitida relies strongly on piloting—leading new foragers from hive to food site during flight (Nieh et al., 2003). Foragers of M. subnitida could be observed to frequently arrive in small groups, while A. mellifera and P. flavocincta workers seemed more independent from each other. Scent marks play an important role for the communication of reward availability, but their impact on recruitment seems dependent on the specific strategy used by species (Free and Williams, 1983; Corbet et al., 1984; Giurfa and Nunez, 1992; Giurfa, 1993; Stout et al., 1998; Stout and Goulson, 2001; Schmidt et al., 2003). The attractiveness of scent marks, whether or not they were used for recruitment purposes, appears to be strong because scent-marked feeders were preferred by all three tested bee species. During the experiments workers foraged in groups and could be influenced by the presence of other individuals. An influence by social facilitation (Wilson, 1971) could not be excluded during the experiments, but when comparing the results for choices of blue and yellow feeders, after the respective training, an influence solely by the presence of conspecifics seems unlikely.

Another aspect that can explain the diverse results for the three tested bee species could be their natural habitat. M. subnitida originates from the Caatinga, which is an open habitat, while P. flavocincta inhabits a spacious habitat that extends from the Caatinga to the Atlantic Rainforest, which is a densely vegetated forest (Imperatriz-Fonseca et al., 2017). Because of its domestication, the honeybee is widespread all over the world. It originates from diverse habitats of Europe, the Middle East, and Africa. Open habitats are brightly illuminated, while forest habitats are characterized by dim-light conditions (Endler, 1992). Based on the light conditions of their respective habitat, it appears to be possible that M. subnitida and A. mellifera could rely to a greater extent on visual signals than P. flavocincta that encounters dim-light conditions and a less visually structured vegetation. In a densely vegetated habitat, scent marks could be a more reliable signal to guide foragers to a food source. Furthermore, temperate and sub-tropical regions experience more distinct seasons concerning weather conditions and the rhythm of flowering plants is directly influenced, while tropical and semi-arid regions have more steady weather conditions but are challenging for their inhabitants because of high temperatures (Prado, 2003; Zanella and Martins, 2003; Machado and Lopes, 2004; Maia-Silva et al., 2012, 2015; Hrncir et al., 2019).

Social bee species that face seasonal variations mass-collect floral resources for provision of the hive (Ramalho, 2004). These variations in floral resource availability could be another explanation for more distinct preferences for visual signals in honeybees when compared to tropical species, like M. subnitida and P. flavocincta, because only honeybees face strong seasonal variations (Michener, 1974; Kleinert-Giovannini, 1982; Roubik, 1982a; Seeley, 1985). Nonetheless, this would not explain the differences between M. subnitida and P. flavocincta.

Conclusion

The three tested bee species reacted vaguely similar to color, scent marks, and location of food sources, but their main focus varies: While A. mellifera choose food sites according to both color and scent marks, M. subnitida orientates on location and color of food sites, and P. flavocincta relies mainly on scent marks. These variations are possibly based on different recruitment mechanisms (e.g., waggle dance of honeybees vs. piloting, excited movements, vibration, and scent mark deposition by stingless bees) or they could be the result of adaptations to the bees’ respective habitat and obliged morphological constraints. Although highly eusocial stingless and honeybees do not communicate the color of flowers to nestmates (Michelsen, 2014), flower color has a large impact on foraging decisions. This impact is demonstrated by the results of this study, that bees exhibit a spontaneous response to color cues and that they memorize color cues following experience; spontaneous response of bees and discrimination after conditioning might rely on different color parameters, such as color saturation and color hue (Rohde et al., 2013). Flower color has also been identified as a floral filter excluding bees from visiting the less preferred flower colors, i.e., red, UV-absorbing and white, UV-reflecting hummingbird-pollinated flowers (Lunau et al., 2011). Stingless bees are known as nectar robbers of hummingbird-pollinated flowers (Roubik, 1982b); it remains to be tested if the less pronounced color preferences in stingless bees are helpful for finding food on flowers displaying colors that are not adapted to bee-color vision and color preferences.

Data Availability Statement

All datasets generated for this study are included in the article/Supplementary Material.

Author Contributions

KL conceived and developed the research concept and supervised the study. SK designed the experiments. MH and KL supported the design of the experiments. SK, VF, LR, and SB conducted the experiments and collected and analyzed the data. SK wrote the manuscript. SB, VF, LR, SB, MH, and KL supported the writing of the manuscript.

Funding

This study was supported by the Deutsche Forschungsgemeinschaft and by CGIAR Research Program on Roots, Tubers, and Bananas and CGIAR Fund Donors.

Conflict of Interest

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.

Acknowledgments

We acknowledge the financial contribution of the CGIAR Research Program on Roots, Tubers, and Bananas and the CGIAR Fund Donors. The study was part of research project about “Color preferences in stingless bees—features of an outstanding visual ecology” (Köthe, 2019) funded by the Deutsche Forschungsgemeinschaft.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2020.00516/full#supplementary-material

FIGURE S1 | Spectral reflectance curves of colored feeders.

TABLE S1 | Position of feeders in training and test phase. The order of tests was pseudo-randomized to ensure no influence of test order on the decisions of workers. Two experimental trials were conducted comprising four choice experiments each. C1–C4 are the tests which focused on blue color, while the tests C5–C8 focused on yellow color. SM1–3 = are tests which analyzed the impact of scent marks; m = marked feeder; u = unmarked feeder; C1–8 = are the tests analyzing the impact of color; b = blue; y = yellow; site 1 = 15 m distance to the hive; site 2 = 17 m distance to the hive.

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Keywords: eusocial bees, chemical cues, color cues, location-dependent cues, foraging behavior

Citation: Koethe S, Fischbach V, Banysch S, Reinartz L, Hrncir M and Lunau K (2020) A Comparative Study of Food Source Selection in Stingless Bees and Honeybees: Scent Marks, Location, or Color. Front. Plant Sci. 11:516. doi: 10.3389/fpls.2020.00516

Received: 05 February 2020; Accepted: 06 April 2020; Published: 06 May 2020.

Eduardo Narbona, Universidad Pablo de Olavide, SpainEdited by:

Islam S. Sobhy, Keele University, United Kingdom Scarlett Howard, Deakin University, AustraliaReviewed by:

Copyright © 2020 Koethe, Fischbach, Banysch, Reinartz, Hrncir and Lunau. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Klaus Lunau, [email protected]

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Front. Plant Sci., 06 May 2020 | https://doi.org/10.3389/fpls.2020.00516

A Comparative Study of Food Source Selection in Stingless Bees and Honeybees: Scent Marks, Location, or Color

📷Sebastian Koethe1, 📷Vivian Fischbach1, 📷Sarah Banysch1, 📷Lara Reinartz1, 📷Michael Hrncir2,3 and 📷Klaus Lunau1*

• 1Institute of Sensory Ecology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
• 2Departamento de Biociências, Universidade Federal Rural do Semi-Árido, Mossoró, Brazil
• 3Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil

In social bees, the choice of food sources is based on several factors, including scent marks, color, and location of flowers. Here, we used similar setups, in which two stingless bee species, Melipona subnitida and Plebeia flavocincta, and the Western honeybee, Apis mellifera, were tested regarding the importance of chemical cues, color cues, and location-dependent cues for foraging behavior. It was determined whether workers chose food sources according to (1) scent marks deposited by conspecifics, (2) the color hue of a food source, (3) the trained location or the proximity of a food source to the hive. All three species preferred the scent-marked over an unmarked feeder that was presented simultaneously, but M. subnitida showed a weaker preference compared to the other species. When trained to blue feeders all three bee species preferred blue, but A. mellifera showed the strongest fidelity. The training to yellow feeders led to less distinct color choices. Only workers of M. subnitida mostly orientated at the training position and the close proximity to the nest. Whether the distance of a feeding site influenced the choice was dependent on the tested parameter (color or scent marks) and the species. Workers of M. subnitida preferably visited the feeder closer to the nest during the scent mark trials, but choose randomly when tested for color learning. Worker honeybees preferred the closer feeding site if trained to yellow, but not if trained to blue, and preferred the more distant feeder during the scent mark trials. Workers of P. flavocincta preferred the closer feeder if trained to blue or yellow, and preferred the more distant feeder during the scent mark trials. The disparity among the species corresponds to differences in body size. Smaller bees are known for reduced visual capabilities and might rely less on visual parameters of the target such as color hue, saturation, or brightness but use scent cues instead. Moreover, the dim-light conditions in forest habitats might reduce the reliability of visual orientation as compared to olfactory orientation. Honeybees showed the most pronounced orientation at floral color cues.

Introduction

Foraging bees use visual and olfactory cues to find and select food sources and deploy innate or learned preferences to detect flowers (Lunau and Maier, 1995; Dyer et al., 2016). Primarily, a forager’s choice is biased by innate preferences for particular colors, shapes, and odors (Menzel, 1967; Giurfa et al., 1995; Lehrer et al., 1995; Lunau et al., 1996; Gumbert, 2000; Biesmeijer and Slaa, 2004; Raine and Chittka, 2007; Howard et al., 2019). These innate preferences differ among species. In several experiments, preferences for specific hues and saturation of colors could be found for honeybees and bumble bees (Lunau, 1990; Giurfa et al., 1995; Lunau et al., 1996; Papiorek et al., 2013; Rohde et al., 2013), while stingless bees sparsely show preferences for color hue or saturation (Spaethe et al., 2014; Dyer et al., 2016; Koethe et al., 2016, 2018).

With increasing foraging experience, initial individual preferences may be either consolidated or modified through associative learning (Gumbert, 2000; Sánchez et al., 2008; Roselino et al., 2016). For instance, species-specific chemical footprints deposited by bees while landing on and manipulating flowers indicate the recent presence of a forager to subsequent visitors (Hrncir et al., 2004; Jarau et al., 2004; Eltz, 2006; Saleh and Chittka, 2006; Witjes et al., 2011). An initial attraction toward the familiar scent of conspecifics (Schmidt et al., 2005) may be reinforced when individuals learn to associate the footprints with high reward levels or reversed when scent marks indicate depleted flowers (Saleh and Chittka, 2006; Roselino et al., 2016).

Learning and memory play a major role in bee foraging, enabling the repeated visit to sustainable food sources (Breed et al., 2002; Reinhard et al., 2004, 2006; Jesus et al., 2014), flower constancy (Free, 1963; Biesmeijer and Toth, 1998; Slaa et al., 1998, 2003), and the discovery of new patches of known food plants (Biesmeijer and Slaa, 2004). In addition to memorizing scent and location of resources (Reinhard et al., 2004, 2006), bees learn both color and position of landmarks, which facilitates the orientation toward food sources and the nest (Cartwright and Collett, 1983; Cheng et al., 1986, 1987; Chittka et al., 1995; Menzel et al., 2005). However, species differ concerning their learning ability (Pessotti and Lé’Sénéchal, 1981; Mc Cabe et al., 2007), which might be associated with differences in life-history and ecological traits among bee species, such as longevity of individuals (Ackerman and Montalvo, 1985), the degree of floral specialization (Cane and Snipes, 2006), and food niche-breath (Biesmeijer and Slaa, 2006).

In eusocial bees, including the stingless bees (Meliponini), bumble bees (Bombini), and honeybees (Apini), food source selection is not only based on individual foraging preferences, but relies to a large extent on social information. On their return to the nest, foragers transmit olfactory and gustatory information about the exploited food source to nestmates, which biases the subsequent food choice of the receivers (Farina et al., 2005, 2007; Mc Cabe and Farina, 2009). Moreover, returning foragers of many species announce the existence of lucrative food sources through thoracic vibrations (stingless bees: Lindauer and Kerr, 1958; Esch et al., 1965; Barth et al., 2008; Hrncir and Barth, 2014; honeybees: Esch, 1961; Waddington and Kirchner, 1992; Hrncir et al., 2011). Inactive individuals may use these mechanical signals for their decision of whether to engage in foraging or to remain in the nest. In addition, foragers of some eusocial bee species guide the recruits to the location of the exploited food patch. Honeybees (all species) use an elaborated dance language (waggle dance) communicating information about distance, direction, and quality of foraging sites (Von Frisch, 1967; Dyer, 2002). Stingless bees (few species), in contrast, lay polarized trails of species-specific pheromone marks that guide recruits with high precision toward the goal (Lindauer and Kerr, 1958; Schmidt et al., 2003; Nieh et al., 2004; Barth et al., 2008; Jarau, 2009). At the food patch, foraging choices are influenced by field-based social information, like olfactory footprints and the visual presence of con- or heterospecific foragers (Slaa et al., 2003). Depending on the composition of the foraging community at the food patch, these passively provided cues may cause local enhancement or local inhibition (Slaa and Hughes, 2009). Thus, food source selection in eusocial species is based on a complex interplay between individual preferences and social information.

Differences among social bee species regarding ecological (habitat, food niche), physiological (learning ability, visual capacity, color vision), and behavioral features (innate preferences, foraging strategy, recruitment mechanism) may result in differences concerning the parameters used in foraging decisions. With more than 500 described species, stingless bees (Meliponini) are the most speciose group of eusocial bees with very diverse characteristics regarding body size, colony size, nesting biology, brood cell arrangement, queen production, foraging strategies, and recruitment mechanisms (Michener, 1974, 2013; Johnson, 1983; Wille, 1983; Engels and Imperatriz-Fonseca, 1990; Roubik, 2006; Barth et al., 2008). Given this biological diversity, we can expect differences concerning the mechanisms of food source selection among species. In the present study, we investigated the food source selection by two stingless bee species, Melipona subnitida and Plebeia flavocincta, and the Western honeybee, Apis mellifera. Since stingless bees show only weak preferences for colors compared to other bee species (Dyer et al., 2016; Koethe et al., 2016, 2018), alternative parameters could be of importance for foraging choices. Of interest were the roles of scent marks (olfactory footprints), the color, and the location of a food source. Melipona species are known to mark food sources with olfactory footprints (Jarau, 2009; Roselino et al., 2016). For P. flavocincta, no specific information concerning scent communication is available so far (Aguilar et al., 2005). However, given that all bee species studied to this moment deposit chemical footprints at food sources (Goulson et al., 1998; Eltz, 2006; Yokoi et al., 2007; Jarau, 2009; Witjes et al., 2011), scent cues can also be postulated for this meliponine species. A. mellifera is known for marking food sources directly (Giurfa and Nunez, 1992).

The aim was to analyze how the three investigated social bee species use the parameters color, scent marks, or location differently during the colony foraging processes. We test the hypothesis that these bees possess a hierarchy in the use of the parameters color, scent marks, and location of flowers. We expect honeybees to rely more on color cues than the two stingless bee species. For the two stingless bee species, we assume that they follow scent markings of conspecifics more reliable than honeybees. Since small stingless bee might exploit nectarrich flowers by repeated visits to the same individual flower, we assume that the location of the flower is of higher importance in the smaller bees.

Materials and Methods

This study is part of a research project on color preferences in stingless bees conducted in Australia and Brazil (Köthe, 2019).

Study Site and Bee Species

The foraging behavior of the stingless bee species was investigated at the Brazilian Federal University at Mossoró (Universidade Federal Rural do Semi-Árido), located in the Brazilian tropical dry forest, the Caatinga at 5°12′13.3″S 37°19′44.8″W. For our experiments, we used two stingless bee species native to the study region, M. subnitida (six colonies) and P. flavocincta (one colony) (Zanella, 2000; Imperatriz-Fonseca et al., 2017). P. flavocincta is the smallest bee with less than 5 mm body length (Cockerell, 1912), M. subnitida is intermediate with 7.5–8.5 mm (Schwarz, 1932), and A. mellifera is the largest with more than 11 mm (Amiet and Krebs, 2012). Colonies of the stingless bee species were kept in wooden nest-boxes at the university’s meliponary (Meliponário Imperatriz) and were freely foraging. The foraging behavior of the Western honeybee, A. mellifera, was studied at the botanical garden of the Heinrich Heine University Düsseldorf, Germany at 51°11′10.7″N 6°48′14.1″E. Foragers of five nests were trained to participate in the experiment. The colony size of the three tested species differs and ranges from several thousand individuals (20.000–80.000) in a single colony of A. mellifera to several hundred (up to 1000) in M. subnitida (Wilson, 1971; Michener, 1974). For P. flavocincta, colony size has not been determined yet, but in other Plebeia species, colony size has been shown to range from 2.000 to 3.000 individuals (Roldão-Sbordoni et al., 2018).

The reasons for conducting the study on stingless bees and honeybees at different study sites were as follows: Most experimental research in Western honeybees has been done in Europe and Australia, excluding the Africanized honeybees available in Mossoro. Moreover, A. mellifera is not native in South America. Thus, direct comparison with literature data is easier when working with European Western honeybees, although direct comparison of foraging strategies in stingless bees and honeybees in the same habitat might also yield interesting results (Roubik and Buchmann, 1984). The origin of the Western honeybee is in the Middle East or Africa (Han et al., 2012) and Western honeybees have developed adaptations to get along with temperate climates (Han et al., 2012).

Bee Training

For all tests and bee species, the training was identical. Workers of all three species were trained to mass feeders offering sugar solution (50%) affixed to tripods. The training to the mass feeders started at the respective nest’s entrance. After more than 10 workers regularly foraged at the feeder, it was moved in short steps (∼1 m) away from the nest until a distance of 15 m (site 1) or 17 m (site 2) was reached. Once at the final feeding site, the mass feeder was replaced by a colored gravity feeder (10 cm diameter, 5 cm height) that was used during the experiment. The gravity feeders were either blue (edding permanent spray RAL5010 enzianblau, edding International GmbH, Ahrensburg, Germany) or yellow (only for the color test; edding permanent spray RAL 1037 sonnengelb, edding International GmbH, Ahrensburg, Germany). The colors were measured using spectrometer analysis (USB4000 miniature fiber optic spectrometer, Ocean Optics GmbH, Ostfildern, Germany) at an angle of 45° using a UV-NIR deuterium halogen lamp (DH-2000-BAL, Ocean Optics GmbH), which was connected to the spectrometer by a UV–VIS fiber optic cable (Ø 600 μm, QR600-7-UV 125 BX, Ocean Optics GmbH). To calibrate the spectrometer, a black standard (black PTFE powder, Spectralon diffuse reflectance standard SRS-02-010, reflectance factor of 2.00%, Labsphere, Inc., North Sutton, NH, United States) and a white standard (white PTFE powder, Spectralon diffuse reflectance standard SRS99-010, reflectance factor of 99.00%, Labsphere, Inc., North Sutton, NH, United States) were used (Supplementary Figure S1). After the workers accepted the colored gravity feeder (henceforth “feeder”), a training period of 30 min started, in which the bees were allowed to forage ad libitum (approximate number of foragers during training phase: M. subnitida ≈ 10 individuals; P. flavocincta ≈ 30–50 individuals, A. mellifera ≈ 30–50 individuals). Workers were not marked during the training to keep the disturbance at the feeder to a minimum. Hence, no discrimination between experienced and inexperienced workers was possible.

Experiments

Testing the Impact of Scent Marks

We conducted experiments investigating the influence of scent marks deposited at the training feeder on the choice behavior of foragers. For this experimental series, we used only blue-colored feeders. In total, we performed three trials with each bee species. In preliminary studies, this approach turned out to be most reasonable for comparative studies between these bee species. Each trial consisted of three sets of a 30-min training phase and a subsequent 5-min test phase, switching the feeder positions in pseudo-randomized order (SM1–SM3; Supplementary Table S1). After the training phase, we offered the incoming bees both the training feeder (scent-marked) and a clean blue-colored feeder (unmarked), one at each feeding site (Supplementary Table S1). During this test phase, both feeders contained sugar solution (50%). In total, we performed three trials of this experimental series with each bee species. A trial consisted of three pairs of a 30-min training phase and a 5-min test phase intermitted by 30-min training phases (SM1–SM32; Supplementary Table S1), switching the feeder positions in pseudo-randomized order. The three different bee species (A. mellifera, M. subnitida, and P. flavocincta) were tested separately. Workers that visited the feeder were either marked with nail polish on their first visit (A. mellifera and M. subnitida) or caught after landing (P. flavocincta) and released at the end of the respective 5-min test phase. Workers were allowed to participate in all three trials. To avoid pseudo-replication (A. mellifera, M. subnitida), only the first landing of an individual in each test phase was considered for the analysis. During the third test, all foragers were captured and killed by freezing to avoid pseudo-replication.

Testing the Impact of Color

In the second experimental series, we investigated the impact of color on the choice of food sites by workers. In this experimental series, we performed two different trial series with each bee species. Each trial consisted of two sets of a 30-min training phase and a subsequent 5-min test phase, switching the feeder positions in pseudo-randomized order (Supplementary Table S1). After the training phase (training feeder either blue or yellow; Supplementary Table S1), the training feeder was removed, and we offered the incoming bees a blue- and a yellow-colored feeder during the test phase, one at each feeding site (Supplementary Table S1). In trial series 1 (C1–C4; Supplementary Table S1), bees were trained to blue feeders in the first three training phases and a yellow feeder in the fourth (training to blue, retraining to yellow). In trial series 2 (C5–C8; Supplementary Table S1), foragers were trained to yellow feeders during three training phases and a blue feeder in the last training phase (training to yellow, retraining to blue). For the test phases, we used alcohol-cleaned feeders to eliminate the influence by any potential scent marks. During the test phase, both feeders offered sugar solution (50% weight on weight). Each trial series was repeated three to five times with different individuals. The bee species (A. mellifera, M. subnitida, and P. flavocincta) were tested separately and workers that visited the feeder were either marked with nail polish (A. mellifera and M. subnitida) or caught after landing on a feeder (P. flavocincta) and released at the end of the respective 5-min test phase. To avoid pseudo-replication (A. mellifera, M. subnitida), only the first landing of an individual in each test was considered for the analysis. During the fourth test, all workers were captured and killed by freezing.

Testing the Impact of Location

To test whether bees visited the feeding site closer to the nest (site 1, 15 m) more often than the farther feeding site (site 2, 17 m) the results of all above described tests (scent marks and color) were analyzed concerning the influence of distance.

Statistics

The statistical program R was used to analyze the data (R Development Core Team, 2019). The data were analyzed by testing the bees’ choices (the first decision of each test) for the different parameters (scent marks, color, distance) using a generalized linear mixed model (GLMM). We used the “lme4” package of R to analyze choices of the bees, which were assessed using GLMM with Poisson distribution of data (Bates et al., 2009; R Development Core Team, 2019). We analyzed the number of choices for each test as fixed effect and the position of the stimuli were used as random effect of the model when testing the influence of color and scent marks, while these parameters were used as random effect when testing the impact of distance on the bees’ choice behavior.

Results

In the first experimental series (influence of scent marks), foragers of all three bee species significantly preferred the previously visited training feeder over the clean feeder (Figure 1; M. subnitida: n = 239, z-value = −8.346, p < 0.001; P. flavocincta: n = 355, z-value = −12.15, p < 0.001; A. mellifera: n = 303, z-value = −10.46, p < 0.001).

FIGURE 1

📷

Figure 1. Landings of workers on a scent-marked and an unmarked feeder. A generalized linear mixed model was used for statistical analysis (∗∗∗p < 0.001).

In the second experimental series, we investigated the influence of color on the feeder choice by the three bee species. After training to a blue-colored feeder, all three species significantly preferred the blue feeder over the yellow feeder (Figure 2A; M. subnitida: n = 250, z-value = −10.24, p < 0.001; P. flavocincta: n = 230, z-value = −8.821, p < 0.001; A. mellifera: n = 538, z-value = −10.85, p < 0.001). When these workers were retrained to forage on a yellow feeder during the last training phase, the two stingless bee species significantly preferred the yellow feeder while honeybee workers visited both colors equally (Figure 2B; M. subnitida: n = 124, z-value = 2.667, p = 0.007; P. flavocincta: n = 71, z-value = 3.756, p < 0.001; A. mellifera: n = 278, z-value = 0.6, p = 0.549). When workers were initially trained to a yellow-colored feeder, both stingless bee species preferred the yellow feeder significantly over the blue feeder during the test, while A. mellifera preferred the blue feeder (Figure 2C; M. subnitida: n = 199, z-value = 3.318 p < 0.001; P. flavocincta: n = 303, z-value = 3.141, p = 0.002; A. mellifera: n = 556, z-value = 5.863, p < 0.001). Retraining to a blue feeder in the last training phase lead to a significant preference of the blue colored feeder in all three species (Figure 2D; M. subnitida: n = 52, z-value = −2.95, p = 0.003; P. flavocincta: n = 61, z-value = −2.632, p = 0.008; A. mellifera: n = 213, z-value = −6.74, p < 0.001).

FIGURE 2

📷

Figure 2. Color choices after training sessions. The three tested bee species were trained to forage on either a blue feeder (A) or a yellow feeder (C). Furthermore, the workers were retrained to the opposite color (B,D). A generalized linear mixed model was used for statistical analysis (∗∗p < 0.01; ∗∗∗p < 0.001; ns = not significant p > 0.05).

When analyzing the influence of the feeders’ positions on the food source choice, we observed that M. subnitida visited the feeding site closer to the nest during the scent mark trials (site 1, 15 m) significantly more often than the farther site (site 2, 17 m) (Figure 3; n = 239, z-value = −8.467, p < 0.001), while choosing randomly when tested for color differences (Figure 3; blue: n = 250, z-value = −0.045, p = 0.964; yellow: n = 199, z-value = 1.502, p = 0.133). Workers of A. mellifera significantly preferred the closer feeding site when they were trained to yellow (Figure 3; n = 556, z-value = −6.147, p < 0.001), but did not distinguish between the two sites when trained for blue (Figure 3; blue: n = 538, z-value = −0.951, p = 0.342; scent marks: n = 199, z-value = −1.502, p = 0.133). In the trial concerning scent marks workers of A. mellifera significantly preferred the farther away feeding site (Figure 3; n = 303, z-value = −10.46, p < 0.001). Workers of P. flavocincta preferred the closer feeding site when trained to blue or yellow (Figure 3; blue: n = 230, z-value = −5.036, p < 0.001; yellow: n = 71, z-value = −4.856, p < 0.001) and significantly visited the farther site when tested concerning scent marks (Figure 3; n = 355, z-value = −2.548, p = 0.011).

FIGURE 3

📷

Figure 3. Landings of workers depending on the feeding site. The number of landings at the feeding sites with 15 m (site 1, black) and 17 m (site 2, white) distance to the hive were compared for A. mellifera, M. subnitida, and P. flavocincta for the two color trials, blue and yellow, and the scent mark trial (generalized linear mixed model *p < 0.05; ***p < 0.001; ns = not significant p > 0.05).

Discussion

The results of this study show that the response to the color of feeder, scent marks, and locations differs among the tested species P. flavocincta, M. subnitida, and A. mellifera. Our results confirm previous findings about the important role of color for food plant detection in honeybees and add further findings to the diverse and sometimes less important role of color for food plant detection in stingless bees. In previous studies of color preferences in stingless bees, the results varied among species. While three species of the genus Melipona chose colors poorly, Tetragonula carbonaria chose colors according to their hue and Partamona helleri showed similar color choices as A. mellifera preferring spectrally purer colors and bluish color hues (Rohde et al., 2013; Dyer et al., 2016; Koethe et al., 2016, 2018). Particularly for the honeybee, it has been shown that besides innate preferences, absolute or differential conditioning and behavioral plasticity play important roles in how they exploit color information (Reser et al., 2012), and that strong color preferences impede learning of other features (Morawetz et al., 2013).

Workers of A. mellifera orientated most strongly according to colors. The blue-colored feeder was preferred in all tests with exception of the retraining to yellow, where A. mellifera showed no depicted choice for one of the two colors and the two stingless bee species preferred the yellow feeder. This is in accordance to previous studies showing that A. mellifera prefers blue colors over other color hues (Giurfa et al., 1995; Horridge, 2007). The two stingless bee species chose feeders according to their colors but rather preferred the feeder color of the previous training. Only when initially trained to yellow they showed weak (M. subnitida) or no preferences for the trained color (P. flavocincta). This preference for blue is in accordance with previous results of stingless bees, but also suggests that it is weaker in stingless bees than in honeybees (Dyer et al., 2016; Koethe et al., 2016). An explanation for less visually driven behavior in stingless bees could be the size differences compared to honeybees. P. flavocincta reaches a body size of 3.6–4.1 mm, M. subnitida of 7.5 mm, and A. mellifera is the largest of the three species with 13–16 mm (Hrncir and Maia-Silva, 2013; Maia-Silva et al., 2015; Imperatriz-Fonseca et al., 2017). Especially the size of the eyes, which is associated with body size, can impact the visual capacities of bees (Streinzer et al., 2016). Workers of P. flavocincta are rather small; consequently, their eyes are also small leading to poorer visual capabilities.

Both stingless bees and honeybees use scent cues to evaluate reward availability of food resources (Nunez, 1967; Butler et al., 1969; Ferguson and Free, 1979; Free and Williams, 1983; Corbet et al., 1984; Giurfa and Nunez, 1992; Giurfa, 1993; Stout et al., 1998; Williams, 1998; Stout and Goulson, 2001). In this study, all three species showed preferences for the marked feeder over the unmarked one. P. flavocincta and A. mellifera chose the marked feeder consistently (∼88% of choices), while M. subnitida preferred the marked feeder, but visited it less frequently (∼64% of choices).

Plebeia flavocincta was the only species that significantly preferred the closer feeding site when tested concerning colors and the farther feeding site when tested regarding scent marks. One interpretation is that P. flavocincta does not differentiate between colors and choses the closer feeding site, while the preference during the scent mark trial could be based on the fact that the scent marked feeder was positioned twice at the farther site and only once at the closer site. In contrast, M. subnitida was the only species in the scent mark trials that visited the food site with shorter distance to the hive more frequently. It seems likely that M. subnitida orientates on location rather than on scent marks. Previous studies showed that species of the genus Melipona mark food sites directly and do not lay scent trails (Hrncir et al., 2004). In order to recruit new foragers, it seems possible that M. subnitida relies strongly on piloting—leading new foragers from hive to food site during flight (Nieh et al., 2003). Foragers of M. subnitida could be observed to frequently arrive in small groups, while A. mellifera and P. flavocincta workers seemed more independent from each other. Scent marks play an important role for the communication of reward availability, but their impact on recruitment seems dependent on the specific strategy used by species (Free and Williams, 1983; Corbet et al., 1984; Giurfa and Nunez, 1992; Giurfa, 1993; Stout et al., 1998; Stout and Goulson, 2001; Schmidt et al., 2003). The attractiveness of scent marks, whether or not they were used for recruitment purposes, appears to be strong because scent-marked feeders were preferred by all three tested bee species. During the experiments workers foraged in groups and could be influenced by the presence of other individuals. An influence by social facilitation (Wilson, 1971) could not be excluded during the experiments, but when comparing the results for choices of blue and yellow feeders, after the respective training, an influence solely by the presence of conspecifics seems unlikely.

Another aspect that can explain the diverse results for the three tested bee species could be their natural habitat. M. subnitida originates from the Caatinga, which is an open habitat, while P. flavocincta inhabits a spacious habitat that extends from the Caatinga to the Atlantic Rainforest, which is a densely vegetated forest (Imperatriz-Fonseca et al., 2017). Because of its domestication, the honeybee is widespread all over the world. It originates from diverse habitats of Europe, the Middle East, and Africa. Open habitats are brightly illuminated, while forest habitats are characterized by dim-light conditions (Endler, 1992). Based on the light conditions of their respective habitat, it appears to be possible that M. subnitida and A. mellifera could rely to a greater extent on visual signals than P. flavocincta that encounters dim-light conditions and a less visually structured vegetation. In a densely vegetated habitat, scent marks could be a more reliable signal to guide foragers to a food source. Furthermore, temperate and sub-tropical regions experience more distinct seasons concerning weather conditions and the rhythm of flowering plants is directly influenced, while tropical and semi-arid regions have more steady weather conditions but are challenging for their inhabitants because of high temperatures (Prado, 2003; Zanella and Martins, 2003; Machado and Lopes, 2004; Maia-Silva et al., 2012, 2015; Hrncir et al., 2019).

Social bee species that face seasonal variations mass-collect floral resources for provision of the hive (Ramalho, 2004). These variations in floral resource availability could be another explanation for more distinct preferences for visual signals in honeybees when compared to tropical species, like M. subnitida and P. flavocincta, because only honeybees face strong seasonal variations (Michener, 1974; Kleinert-Giovannini, 1982; Roubik, 1982a; Seeley, 1985). Nonetheless, this would not explain the differences between M. subnitida and P. flavocincta.

Conclusion

The three tested bee species reacted vaguely similar to color, scent marks, and location of food sources, but their main focus varies: While A. mellifera choose food sites according to both color and scent marks, M. subnitida orientates on location and color of food sites, and P. flavocincta relies mainly on scent marks. These variations are possibly based on different recruitment mechanisms (e.g., waggle dance of honeybees vs. piloting, excited movements, vibration, and scent mark deposition by stingless bees) or they could be the result of adaptations to the bees’ respective habitat and obliged morphological constraints. Although highly eusocial stingless and honeybees do not communicate the color of flowers to nestmates (Michelsen, 2014), flower color has a large impact on foraging decisions. This impact is demonstrated by the results of this study, that bees exhibit a spontaneous response to color cues and that they memorize color cues following experience; spontaneous response of bees and discrimination after conditioning might rely on different color parameters, such as color saturation and color hue (Rohde et al., 2013). Flower color has also been identified as a floral filter excluding bees from visiting the less preferred flower colors, i.e., red, UV-absorbing and white, UV-reflecting hummingbird-pollinated flowers (Lunau et al., 2011). Stingless bees are known as nectar robbers of hummingbird-pollinated flowers (Roubik, 1982b); it remains to be tested if the less pronounced color preferences in stingless bees are helpful for finding food on flowers displaying colors that are not adapted to bee-color vision and color preferences.

Data Availability Statement

All datasets generated for this study are included in the article/Supplementary Material.

Author Contributions

KL conceived and developed the research concept and supervised the study. SK designed the experiments. MH and KL supported the design of the experiments. SK, VF, LR, and SB conducted the experiments and collected and analyzed the data. SK wrote the manuscript. SB, VF, LR, SB, MH, and KL supported the writing of the manuscript.

Funding

This study was supported by the Deutsche Forschungsgemeinschaft and by CGIAR Research Program on Roots, Tubers, and Bananas and CGIAR Fund Donors.

Conflict of Interest

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.

Acknowledgments

We acknowledge the financial contribution of the CGIAR Research Program on Roots, Tubers, and Bananas and the CGIAR Fund Donors. The study was part of research project about “Color preferences in stingless bees—features of an outstanding visual ecology” (Köthe, 2019) funded by the Deutsche Forschungsgemeinschaft.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2020.00516/full#supplementary-material

FIGURE S1 | Spectral reflectance curves of colored feeders.

TABLE S1 | Position of feeders in training and test phase. The order of tests was pseudo-randomized to ensure no influence of test order on the decisions of workers. Two experimental trials were conducted comprising four choice experiments each. C1–C4 are the tests which focused on blue color, while the tests C5–C8 focused on yellow color. SM1–3 = are tests which analyzed the impact of scent marks; m = marked feeder; u = unmarked feeder; C1–8 = are the tests analyzing the impact of color; b = blue; y = yellow; site 1 = 15 m distance to the hive; site 2 = 17 m distance to the hive.

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Keywords: eusocial bees, chemical cues, color cues, location-dependent cues, foraging behavior

Citation: Koethe S, Fischbach V, Banysch S, Reinartz L, Hrncir M and Lunau K (2020) A Comparative Study of Food Source Selection in Stingless Bees and Honeybees: Scent Marks, Location, or Color. Front. Plant Sci. 11:516. doi: 10.3389/fpls.2020.00516

Received: 05 February 2020; Accepted: 06 April 2020; Published: 06 May 2020.

Eduardo Narbona, Universidad Pablo de Olavide, SpainEdited by:

Islam S. Sobhy, Keele University, United Kingdom Scarlett Howard, Deakin University, AustraliaReviewed by:

Copyright © 2020 Koethe, Fischbach, Banysch, Reinartz, Hrncir and Lunau. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Klaus Lunau, [email protected]

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A Comparative Study of Food Source Selection in Stingless Bees ...

https://www.frontiersin.org/articles/10.3389/fpls.2020.00516/full

This scientific research article in Frontiers in Ecology and Evolution was published in 2021 and concentrates on "eusocial bees"; the prefix "eu-" denotes "good"!

"ORIGINAL RESEARCH article

Front. Ecol. Evol., 04 August 2021 | https://doi.org/10.3389/fevo.2021.708178

Foraging and Drifting Patterns of the Highly Eusocial Neotropical Stingless Bee Melipona fasciculata Assessed by Radio-Frequency Identification Tags

📷Ricardo Caliari Oliveira1*†, 📷Felipe Andrés León Contrera2†, 📷Helder Arruda3,4, 📷Rodolfo Jaffé4,5, 📷Luciano Costa4, 📷Gustavo Pessin4,6,7,8, 📷Giorgio Cristino Venturieri9,10, 📷Paulo de Souza11 and 📷Vera Lúcia Imperatriz-Fonseca4,12

• 1Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Leuven, Belgium
• 2Laboratório de Biologia e Ecologia de Abelhas – Instituto de Ciências Biológicas, Universidade Federal do Pará – Rua Augusto Corrêa, Belém, Brazil
• 3Polytechnic School, Universidade do Vale do Rio dos Sinos, São Leopoldo, Brazil
• 4Vale Institute of Technology – Sustainable Development, Rua Boaventura de Silva, Belém, Brazil
• 5Exponent, Bellevue, WA, United States
• 6Vale Institute of Technology – Mining, Ouro Preto, Brazil
• 7Institute of Exact and Natural Sciences, Federal University of Pará, Belém, Brazil
• 8Computing Department, Universidade Federal de Ouro Preto, Ouro Preto, Brazil
• 9Nativo Bees, Brisbane, QLD, Australia
• 10Embrapa Amazônia Oriental, Belém, Brazil
• 11School of Information Communication Technology, Griffith University, Gold Coast, QLD, Australia
• 12Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil

Bees play a key role in ecosystem services as the main pollinators of numerous 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 habitat and to the climate. Here, we used radio-frequency identification tags to monitor the foraging behavior of the neotropical stingless bee Melipona fasciculata with special interest in drifting patterns i.e., when a forager drifts into a foreign nest. In addition, we collected meteorological data to study how abiotic factors affect bees’ activity and behavior. Our results show that only 35% of bees never drifted to another hive nearby, and that factors such as temperature, humidity and solar irradiation affected the bees drifting rates and/or foraging activity. Moreover, we tested whether drifting levels would decrease after marking the nest entrances with different patterns. However, contrary to our predictions, there was an increase in the proportion of drifting, which could indicate factors other than orientation mistakes playing a role in this behavior. Overall, our results demonstrate how managed bee populations are affected by both nearby hives and climate factors, offering insights on their biology and potential commercial application as crop pollinators.

Introduction

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.

Materials and Methods

Study Species and Experimental Design

This study was performed with the stingless bee Melipona fasciculata, which has its natural distribution in the northern region of Brazil (Pedro, 2014). The colonies used in the experiment were located at the meliponary of Eastern Amazon Embrapa, in an environment consisting of a mosaic of agricultural crops, forest remnants, and human habitations, where worker bees could forage freely on their expected range of about 2.5 km (Van Nieuwstadt and Iraheta, 1996; Araujo et al., 2004; Kuhn-Neto et al., 2009; Nunes-Silva et al., 2019). The climate at the site is characterized as tropical with daily mean precipitation of at least 60 mm throughout the year (Alvares et al., 2013).

To analyze the foraging and drifting patterns of M. fasciculata, eight experimental colonies were housed in identical hives designed for stingless bees and located in a shed consisting of two parallel rows with four colonies each that were placed 15 cm apart (Figure 1A). A plastic tube that extended the colony entrance and allowed the positioning of the antennae and microcomputer of the RFID system was placed in the front of the hive. The entire system was enclosed inside a box that protected entrance tubes from direct light in order to not disturb the forager’s behavior (Figure 1B). Young worker bees that were not yet foraging were randomly sampled from each hive to receive the RFID tags. Bees were tagged every week for 9 consecutive sessions with 40 workers tagged per week, amounting to 360 bees per colony and 2,880 in total. The process consisted in collecting the young workers in the early morning (8:00–9:00) and placing them in a tube with maximum 5 workers per tube prior to tagging them with the RFIDs. The RFID-tags were then glued with cyanoacrylate adhesive onto the worker thorax (Figure 2B) and, after all bees were marked and the glue sufficiently dried, they were returned to their original hive. Workers from M. fasciculata tolerated well the RFID-tags glued on their thorax without any apparent disturbance to their flight behavior (Nunes-Silva et al., 2019; Gomes et al., 2020; Costa et al., 2021). Finally, after 42 days of the beginning of the experiment, colonies received simple geometrical individual black and white markings made with electrical tape at their entrances to test whether foragers would then improve recognition of their own hive and drift to fewer foreign hives, i.e., make fewer orientation mistakes. The experiment ran for another 78 days after the marking of the colony entrances until the activity of tagged bees was no longer observed. Despite the unbalanced number of days before and after marking the colony entrances, the number of worker bees tracked during each period was similar (n = 1496 workers during control and n = 1,203 during the experimental period).

FIGURE 1

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Figure 1. (A) Experimental setup scheme not to scale with four hives in the 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 containing the RFID system. 1, box containing the Intel Edison and Breakout Board; 2, RU-824 antenna; 3, tube connecting the hive to the entrance, and 4, protective plastic casing.

FIGURE 2

📷

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.

RFID-System Setup

This study was conducted using the Radio Frequency Identification System Ultra Small Package Tag (USPT) developed by Hitachi Chemical (Endou et al., 2014). The system consisted in a single antenna placed below the colony entrance tube connected to an Intel Edison micro-computer to store data (Figure 1B). Each tag was recorded with an individual ID that included the bee number and her colony of origin prior to being glued onto the bees. Therefore, whenever a tagged bee passed through the entrance tube both worker ID and time of the day were recorded. A caveat of the experimental design was that our system consisted of only one reader per 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. Moreover, guard bees staying by the colony entrance would have repeated readings over a short period of time. Hence, only signals that were at least 180 s apart were included in the analysis to resolve this issue. Thresholds between 60 s and 5 min are consistently used to filter RFID foraging data in Hymenoptera (Lach et al., 2015; Dosselli et al., 2016; Susanto et al., 2018; Santoro et al., 2019). This threshold was adopted during data filtering in order to reflect only the extranidal flight activity. We opted for this threshold because, while it might misrepresent short patrolling flights, it prevents overestimating their foraging activity.

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 Criterion. The selected best model had drifting numbers coded as the dependent variable with activity span, hive ID, number of days to begin foraging as well as several meteorological factors coded as covariates with a Poisson error distribution. We then 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. In addition, we tested whether the proportion of drifters present on the colonies was different before and after marking the colony entrances by fitting a binomial GLMM with the proportion of 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 with overdispersion as random factors. Finally, we tested whether drifters had any preference on the direction they would drift. To this end, we ran a binomial GLM with the direction of the drifting event (i.e., horizontal and vertical) as the dependent variable, both the natal hives ID and the host hives ID as cofactors and individual IDs as a random factor. When appropriate, models were tested for temporal autocorrelation, which was not observed in the data. The R script used in the analyses as well as the original datasets are publicly available in the data repository (Oliveira et al., 2021). All models presented in the results section are Poisson GLMs unless otherwise specified. In addition, Wald Z Scores are shortened to Z throughout the text.

Results

Bees Extranidal Activity

Our results show that the tagged workers were active on average for 9.3 days, ranging from a minimum of 1.2 to a maximum of 72.5 days after being tagged (Figure 2A). In addition, bees began foraging on average 2 days after being tagged, with some more extreme cases where workers only started foraging after 25 days and beyond, as registered by the first reading of their tags at the colony entrance (Figure 2C). Foragers were active throughout the day, with most activity being recorded during the early morning hours (between 5:00–10:00), reaching the peak activity at 9:00 and then decreasing until 18:00 (Figure 2D). Furthermore, our data show that workers in colony four showed significantly less activity, while in colony one and two significantly more activity than the average was recorded (colony four: Z = −7.602, p < 0.001; colony one: Z = 2.373, p = 0.047; colony two: Z = 5.478, p < 0.001). Figure 3 illustrates the reconstructed foraging activity of all 2,880 bees during the 4-month study period.

FIGURE 3

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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.

Factors Affecting Drifting Behavior and Foraging Activity

Throughout the study period, 64.1% of all tagged workers drifted to at least one other colony, with 36.6% drifting to only one, 19.1% to two, 7.6% to three foreign colonies, and the percentage decreasing below 1% as the number of foreign colonies increased up to a maximum of seven colonies, i.e., all non-natal experimental colonies (Figure 4A). It is interesting to note that the majority of the drifting events was in the horizontal plane, that is, workers mostly drifted to colonies on their left or right rather than above or below their natal hives (Binomial GLMM, Z > 8.568, p < 0.001 for all colonies, Figure 4B). Moreover, colonies placed on both edges produced fewer drifters than colonies placed between other hives. For instance, foragers in colonies two, three, six and seven showed significantly higher levels of drifting behavior (hive two: Z = 11.880, p < 0.001; hive three: Z = 11.499, p < 0.001; hive six: Z = 4.125, p < 0.001 and 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, p < 0.001), with hive one being not significant (Z = 0.181, p = 0.936). Furthermore, drifting rates were positively correlated with workers’ lifespan Z = 18.113, p < 0.001) and the sooner bees began foraging after being tagged the higher the observed drifting rates (Z = 7.494, p < 0.001).

FIGURE 4

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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.

In addition to biotic factors, several meteorological factors influenced the levels of drifting behavior, with dew point positively affecting the drifting rates (Z = 3.205, p = 0.001), while solar irradiation (Z = −2.804, p = 0.005), maximum relative humidity (Z = −2.883, p = 0.002) and minimum daily temperature (Z = −2.722, p = 0.006) were negatively correlated to the drifting rates.

During the experimental period colony entrances received individual markings to test whether foragers would then improve recognition of their own hive and drift to fewer foreign hives, i.e., make fewer orientation mistakes. Intriguingly, we observed an increase in the proportion of drifting events after marking the hive entrances, with 63.9% of tagged bees drifting before and 68.7% after the hive entrances were marked (Binomial GLMM, Z = 2.508, p = 0.012), which could indicate factors other than mere orientation mistakes playing a role in drifting behavior (Figure 4A).

Finally, it was possible to observe that meteorological factors were also correlated with the workers extranidal activity, whereby maximum daily atmospheric pressure and temperature, precipitation as well as dew point temperature were positively correlated with the bees activity span (max atmospheric pressure: Z = 6.521, p < 0.001; max temperature, Z = 5.236, p < 0.001; precipitation, Z = 3.020, p = 0.002; max dew point: Z = 2.504, p = 0.012; min dew point: (Z = 4.710, p < 0.001). Conversely, minimum daily temperature and atmospheric pressure, humidity and wind speed negatively affecting the bees’ activity (min temperature: Z = −8.834, p < 0.001; min atmospheric pressure, Z = −6.922, p < 0.001; max humidity: Z = −4.235, p < 0.001; min humidity: Z = −3.156, p = 0.001; and wind speed: Z = −9.901, p < 0.001). Table 1 summarizes the relationship of abiotic factors with both drifting behavior and foraging activity.

TABLE 1

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Table 1. Abiotic factors affecting both drifting behavior and foraging activity.

Discussion

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.

Data Availability Statement

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

Author Contributions

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.

Funding

This project was funded by the Brazilian National Council for Scientific and Technological Development CNPq, grant 444384/2018-9; and by individual research grants to VLIF (CNPq 312250/2018-5), RF (CNPq 301616/2017-5) and RCO (Research Foundation Flanders FWO research Grant 1502119N and postdoctoral Grant 12R9619N).

Conflict of Interest

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.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

We would like to thank Elisângela Rêgo for helping to tag the bees.

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Keywords: stingless bee, radio-frequency identification, Melipona fasciculata, foraging activity, drifting behavior

Citation: Oliveira RC, Contrera FAL, Arruda H, Jaffé R, Costa L, Pessin G, Venturieri GC, de Souza P and Imperatriz-Fonseca VL (2021) Foraging and Drifting Patterns of the Highly Eusocial Neotropical Stingless Bee Melipona fasciculata Assessed by Radio-Frequency Identification Tags. Front. Ecol. Evol. 9:708178. doi: 10.3389/fevo.2021.708178

Received: 11 May 2021; Accepted: 15 July 2021; Published: 04 August 2021.

Isabel Marques, University of Lisbon, PortugalEdited by:

M. N. Kuperman, Bariloche Atomic Centre (CNEA), Argentina Jose Octavio Macias-Macias, University of Guadalajara, Mexico William G. Meikle, Agricultural Research Service, United States Department of Agriculture, United States Reviewed by:

Copyright © 2021 Oliveira, Contrera, Arruda, Jaffé, Costa, Pessin, Venturieri, de Souza and Imperatriz-Fonseca. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Ricardo Caliari Oliveira, [email protected]

†These authors have contributed equally to this work

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher. "

Foraging and Drifting Patterns of the Highly Eusocial Neotropical ...

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The National Institutes of Health (NIH) in the United States of America recognizes the importance of bees, whether stingless or otherwise, to the ecological health of the planet, which naturally includes the human populations which inhabit it. This is only one of a number of scientific research articles which are devoted to this crucial area of scientific research:

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Journal List Biomolecules v.10(6); 2020 Jun PMC7356725 📷 Biomolecules. 2020 Jun; 10(6): 923.Published online 2020 Jun 18. doi: 10.3390/biom10060923PMCID: PMC7356725PMID: 32570769Antioxidant-Based Medicinal Properties of Stingless Bee Products: Recent Progress and Future Directions Mohammad A. I. Al-Hatamleh,1 Jennifer C. Boer,2 Kirsty L. Wilson,2 Magdalena Plebanski,2 Rohimah Mohamud,1,3 and Mohd Zulkifli Mustafa 3,4,*Author information Article notes Copyright and License information DisclaimerThis article has been cited by other articles in PMC.

Abstract

Stingless bees are a type of honey producers that commonly live in tropical countries. Their use for honey is being abandoned due to its limited production. However, the recent improvements in stingless bee honey production, particularly in South East Asia, have brought stingless bee products back into the picture.

Although there are many stingless bee species that produce a wide spread of products, known since old eras in traditional medicine, the modern medical community is still missing more investigational studies on stingless bee products. Whereas comprehensive studies in the current era attest to the biological and medicinal properties of honeybee (Apis mellifera) products, the properties of stingless bee products are less known.

This review highlights for the first time the medicinal benefits of stingless bee products (honey, propolis, pollen and cerumen), recent investigations and promising future directions.

This review emphasizes the potential antioxidant properties of these products that in turn play a vital role in preventing and treating diseases associated with oxidative stress, microbial infections and inflammatory disorders. Summarizing all these data and insights in one manuscript may increase the commercial value of stingless bee products as a food ingredient.

This review will also highlight the utility of stingless bee products in the context of medicinal and therapeutic properties, some of which are yet to be discovered.

Keywords: stingless bee, meliponines, honey, propolis, natural products, phenolic compounds, flavonoids, antioxidants.

1. Introduction Stingless bees (Meliponines) belong to the genus Apidae, which is a family of social bees from the superfamily Apoidea.

Stingless bees are the highest developed species of bees that have been identified in 80 million years old parts of amber [1].

Reports of ancient populations using honey both for nutritional and medicinal properties can be traced back to nearly 5500 years ago [2].

Hand collecting honey bees was an important traditional practice in many ancient populations as it was the only way to get honey and it still persists among some people in forest areas [1].

To date there are more than 500 known stingless bee species, of which approximately 40 species have good potential as honey producers [3,4].

These species are distributed in the tropical and subtropical regions as follows: approximately 391 species in the Neotropical region of South America, 60 in the Indo-Malayan region of Asia, 50 in the Paleotropical region of Africa and 10 in the Australasia region of Australia [5].

Constructing nests in hollow tree trunks or roots, soil cavities or empty animal narrow nests is typical for many stingless bee honey (SBH) producer species [1].

As pollinators, stingless bees play an important role in the forest ecosystem by strongly influencing plant community, diversity and evolution.

The most common species producing SBH are classified under two main genera, Melipona and Trigona [6].

While stingless bees are one of the most common types of honey producers, the distribution of SBH is lower compared to the more common honey produced by Apis mellifera bees (European/Western bees or honeybees) [7], which has been associated with the limited data about SBH production and its properties. Interestingly, SBH is less used as a nutritional and medicinal product [8], despite its higher nutritional and medicinal properties compared to the commonly used honeybee products (European/Western honey) [9,10,11,12].

It is believed that stingless bee products are superior promising sources of biologically active compounds over honeybees, and this can be attributed to the rich vegetation in the tropical and subtropical regions where stingless bees are found [7].

In addition, stingless bees have some principal characteristics that make them unique compared to honeybees, for example they are less vulnerable to disease (Figure 1). Recent evidence indicates that SBH has potential therapeutic benefits in several contexts, including wound healing, diabetes mellitus, eye diseases, hypertension, fertility defects, cancer, microbial infection and dysregulated lipid profiles [13].

Therefore, promoting the research on SBH would help improve the knowledge on its putative medicinal properties and ensure the conservation of SBH trade.

📷Figure 1Principal characteristics of stingless bees that differentiate them from honeybees [7].

It is important to note that stingless bee products are not restricted to honey, but can involve several products including propolis, beebread, cerumen and bee pollen (Figure 2).

Although these are not as common as honey, studies have reported several medicinal properties in those products too [14,15,16]. Based on a comparison between the studies on stingless bees and honeybees, a significant gap in research on stingless bee products has been identified compared to the common honeybee products that are well-studied (Figure 3). Interestingly, in 2019, approximately double the number of studies on stingless bees were reported (Figure 3).

To improve the awareness on the stingless bee, its products, properties, benefits and future opportunities, this manuscript provides a comprehensive review and recent updates on the medicinal properties of stingless bee products.

We also highlight the importance of increasing research investments into stingless bee products for future medical research, as well as to motivate their production and nutritional usage.

📷Figure 2Hive box containing colony of stingless bees (Heterotrigona itama). A, cerumen; B, empty propolis pot; C, honey; D, bee pollen; E, fermented pollen (beebread).

📷Figure 3A comparison between the annual publications on both stingless bees and honey bees in the recent 10 years. Applied on PubMed database on May 9, 2020, by using search terms: (Honeybee; Honey bee; Apis; European bee; Western bee) and (Stingless bee; Melipona; Trigona).

2. Harvesting and Characterization of Stingless Bee Products The percentages of stingless bee products in the beehive are still unknown; it supposed to be varied according to the species. Generally, propolis is main content of stingless bee hive, regardless the species, as the hive is constructed with it [17]. A study on nine Trigona species reported that the hive products of those species were 63.7% propolis, 20.9% beebread and 15.4% honey [18].

Furthermore, the proportion of use for each stingless bee product in the medicinal/commercial industry is also unknown.Stingless bees produce their honey and store it in small resin pots in the hive. In traditional practices, honey pots were commonly squeezed to obtain the honey [19].

This method led to several disadvantages such as damaging the pot and reducing the productivity of the bees. In fact, honey obtained by squeezing the pot produced SBH contaminated with bee bread, which promoted souring of the honey and produced inconsistent honey products [20].

To overcome this, current practices in stingless beekeeping promote the hiving method with a monolayer honey pot induction system that utilizes suction pumps to aspirate the honey pot by pot without damaging the pots [21].

This method produces absolute and hygienic honey as well as supporting sustainable stingless beekeeping. However, so far there are no standard methods for harvesting other stingless bee products.

Beekeepers harvest each of these products by removing it directly from the hive. Menezes et al. have suggested a good method for harvesting unfermented pollen from stingless bees by moving a colony of stingless bees to a another location and stimulate the foragers to accept a new hive, build new pots and leaving the old hive empty [22]. After a week they easily and precisely harvested the pollen from the pots of empty hive.

Despite an improvement in harvesting practices and post-harvest management of SBH, stingless bee products display variability in chemical composition associated with botanical and geographical origin, bee species and climate.

Therefore, a standard characterization worldwide for stingless bee products is not available. However, Malaysia has specifically developed the first SBH standard referred to as Malaysian standard (MS) 2683:2017 [23]. It is used in local regulations according to several parameters including moisture content (

Since this ResearchGate discussion thread question expresses an interest in the stingless bee scientific research in many different parts of the world, here is an interesting survey article which summarizes different studies that cover different types of stingless bees which are located in different locales:

https://www.sciencedirect.com/topics/agricultural-and-biological-sciences/stingless-bees

"Stingless Bees Stingless bees (Meliponinae) reproduce similarly to solitary bees: an egg is laid on top of a food mass in a single cell, which is then sealed (Roubik, 2006; Sakagami, 1982).

From: Advances in Insect Physiology, 2015 Related terms: Pollen Pollinator Pollination Wasp Propolis Honey Bees Biodiversity Nectar Larvae Apis mellifera View all Topics

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Nutraceutical and medicinal properties of native stingless bees honey and their contribution to human health Jesús F. Martínez-Puc, ... Miguel A. Magaña-Magaña, in Functional Foods and Nutraceuticals in Metabolic and Non-Communicable Diseases, 2022

Medicinal properties NSB honey has been used for its medicinal properties since ancient times in Mexico by various indigenous groups, mainly the Zapotecos, Mixes, and Zoques of the Isthmus of Tehuantepec [27].

NSB honey has been used in traditional medicine to treat diseases such as pharyngitis, respiratory tract infections, and eye infections [2,23,28].

Recently, an interest has emerged in verifying the various therapeutic qualities of NSB honey for their anti-inflammatory, antibacterial, healing, and antioxidant properties [10,29]. The most interesting quality is antimicrobial activity, since that could give NSB honey clinical application [29].

Furthermore, the NSB honeys are used to feed women in the postpartum recovery period [23]. Currently, there has been no study that indicates all the benefits that NSB honeys provide in the area of health (Table 33.3) [23,30].

The healing and medicinal effects of these honeys have been applied to a wide range of diseases or conditions; in this sense, it is important to mention that the healing properties of honeys are rooted in people’s beliefs and traditional knowledge [31].

Table 33.3. Main medicinal uses of native stingless bee honey.

Species

Medicinal uses

Melipona beecheii Digestive disorders, eye diseases, respiratory infections, postpartum recovery, fatigue, ulcers, Melipona favosa Labor enhancerMelipona paraensis Postpartum recovery Melipona trinitatis Gastritis Scaptotrigona mexicana Respiratory infections Nannotrigona perilampoides Cataracts, stomach aches, bruises Plebeia jatiformis Cataracts, stomach pains, external head injuries Trigona angustula Stomach disorders, cataracts, respiratory infections, wound healing Based on Vit P, Medina M, Enríquez E. Quality standards for medicinal uses of Meliponinae honey in Guatemala, México and Venezuela. Bee World 2004;85:2–5.

View chapterPurchase book Comb Architecture of the Eusocial Bees Arises from Simple Rules Used During Cell Building Benjamin P. Oldroyd, Stephen C. Pratt, in Advances in Insect Physiology, 2015 8.1 General Plan of a Stingless Bee Nest Stingless bees (Meliponinae) reproduce similarly to solitary bees: an egg is laid on top of a food mass in a single cell, which is then sealed (Roubik, 2006; Sakagami, 1982). Stingless bees have an amazing variety of nest types (Rasmussen and Camargo, 2008; Wille and Michener, 1973). Typically, but not always, stingless bee colonies nest in a cavity. The brood area comprises a dense aggregation of brood cells that is usually surrounded by a covering of multilayered wax and resin called the involucrum, the purpose of which is to protect the brood nest and insulate it (Fig. 11). Outside the involucrum, there is an area of large waxen storage pots where the bees store pollen and honey. The nest is often sealed off from the rest of the cavity by one or more plates of resin called the batumen plates. The nest can be connected to the outside via a waxen entrance tube, which may extend into the air for many centimetres (Fig. 12).X-ray image courtesy of Dr. M. Greco.

📷Sign in to download full-size imageFigure 11. The internal architecture of a typical stingless bee nest (Tetragonula carbonaria). The spiral brood comb is in the centre, surrounded by storage cells, connecting involucrum, and insulating batumen.Photo by B. Oldroyd. 📷Sign in to download full-size imageFigure 12. The entrance tube of a Trigona collina colony.

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Breeding Genetics and Biotechnology D.E. Pattemore, in Encyclopedia of Applied Plant Sciences (Second Edition), 2017 Stingless Bees

Colonial stingless bees (in the bee tribe Meliponini) have been managed for thousands of years in Central America. Many other species are found in South America, Africa, Asia, and Australia, and different traditions of beekeeping are found across these continents. Although management techniques remain primitive compared with the commercial honeybee industry, these bees are increasingly being introduced into orchards for pollination. An industry based around managing colonies of a stingless bee species (Tetragonula carbonaria) in Australia has provided growers with another option for a managed pollinator species in that country.

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Endocrine Control of Insect Polyphenism K. Hartfelder, D.J. Emlen, in Insect Endocrinology, 2012 11.3.3.3.2.4 Hormonal control of caste development and reproduction in stingless bees

The stingless bees are not only closely related to the monogeneric tribe Apini, but are also represented by an enormous number of species (Camargo and Pedro, 1992). Thus, they supply us with ample material for evolutionary insights into caste polyphenism and reproduction in highly social bees. As previously mentioned, it is the nutritional conditions that serve as the initial trigger in the divergence of the queen/worker developmental pathways, even though there is strong evidence for a genetic predisposition to caste fate in the genus Melipona (see Section 11.3.3.3.2.).

As in the honey bee, the initial investigations on the role of hormones in stingless bee caste differentiation all relied on JH application experiments. These comparative investigations on different species of stingless bees (Bonetti et al., 1995; Buschini and Campos, 1994; Campos, 1978, 1979; Campos et al., 1975) established the spinning stage of the last larval instar as the critical phase for JH-dependent induction of queen development. These findings subsequently received support from investigations on CA activity and JH titer measurements in Scaptotrigona postica (Hartfelder, 1987; Hartfelder and Rembold, 1991).

These results indicated that JH-dependent differentiation steps in queen development occur much later in stingless bees when compared to the honey bee (Hartfelder, 1990; Figure 11).

Also, queen development in the trigonine species takes longer than worker development, with the opposite rue for honey bees and the genus Melipona, indicating that the differences in nutritional programs among the three groups (Apis, Melipona, Trigonini) are reflected in larval and especially pupal ecdysteroid titers (Hartfelder and Rembold, 1991; Pinto et al., 2002), arguing for a correlated regulation of caste development by JH and ecdysteroid in these groups of highly social bees.

The high species diversity in the stingless bees, their variation in colony size, nesting sites, and a large number of further aspects in social lifestyles, obviously provide ample material for variation on the basic themes of caste development, reproduction and division of labor, and possible hormonal regulation therein.

An important difference between honey bees and stingless bees lies in the degree of morphological differences between the sexes and castes. The males of stingless bees are morphologically much more similar to workers than they are to queens (Kerr, 1987, 1990), even though growth rules for the different morphogenetic fields along the body axes appear to be adjusted rather independently (Hartfelder and Engels, 1992).

A striking phenomenon calling for functional explanations is the strong variation in queen size in some species. The occurrence and reproductive performance of miniature queens was closely studied and compared to normal-sized queens (Ribeiro et al., 2006), indicating functional differences in reproductive performance related to colony conditions.

Since monopolization of reproduction by the queen is a key element in the social evolution of bees, the large variation in reproductive activities by the workers among stingless bee species can provide insight into different evolutionary solutions to the queen–worker and also the worker–worker conflict over reproduction.

Worker oviposition can take two forms:

(1) trophic eggs that are laid shortly before the queen oviposits and (2) reproductive eggs that are laid after the queen’s oviposition.

Trophic eggs are unviable eggs that are specially produced as nutrition for the queen serving to maintain her high reproductive rates. Worker vitellogenin is, thus, directly shunted into egg production by the queen. Since the production of (trophic) worker eggs is clearly in the interest of the queen, she does not discourage workers to produce these unviable eggs and thus should keep the workers’ ovaries in an active state. It is therefore not surprising that workers can also produce viable eggs that can make a significant contribution to male production in a colony (Cepeda, 2006; Engels and Imperatriz-Fonseca, 1990; Velthuis et al., 2005).

Some species, such as Frieseomelitta varia have, however, opted for a completely different solution to this conflict over reproduction, as their workers are completely sterile due to the complete degeneration of their ovariole anlagen during pupal development (Boleli et al., 1999, 2000).

All the more surprising, on first sight, but consistent with the evolutionary transitions implicit in the reproductive ground plan hypothesis, vitellogenin expression in this ovary-less stingless bee was practically constitutive both at the transcript and at the protein level (Dallacqua et al., 2007; Hartfelder et al., 2006).T

he involvement of hormones in the regulation of reproduction and division of labor in adult stingless bee queens and workers has only marginally been investigated, and so far there is only negative evidence to this end in Melipona quadrifasciata. As in the honey bee, ecdysteroids do not seem to play any role in queen or worker reproduction in M. quadrifasciata (Hartfelder et al., 2002).

Interestingly, however, analyses of ultraspiracle gene homologues in M. scutellaris and S. depilis (Teles et al., 2007) showed differences in pupal transcript levels that might be related to differences in reproductive strategies seen in adult workers of trigonine and Melipona species (Velthuis et al., 2005).

Genomic resources are still scarce for stingless bees, with the exception of M. quadrifasciata, for which a suppression subtractive library analysis has revealed 337 unique sequences as differentially expressed between newly emerged queens and workers (Judice et al., 2006). This situation is, however, bound to change as efforts are under way to generate 454 sequence data for at least two stingless bee species.

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Trigona Propolis and Its Potency for Health and Healing Process Ahmad Sulaeman, ... Mahani Mahani, in The Role of Functional Food Security in Global Health, 2019

25.2 Trigona Species Distribution and Plant Origin

There are so many species of stingless bee around the world. In Indonesia, our identification found more than 30 species of stingless bee around the archipelagos, especially from Trigona species. Most of them are still wild and underutilized. We have observed Trigona species in 10 provinces of Indonesia that have beensuccessfuly cultivated. Among them, there are eight species that productively yield propolis (Table 25.1).Table 25.1. List of Trigona Bee Species Cultivated in 10 Provinces of Indonesia (Sulaeman et al. [5])

No. / Province / Origin / Trigona Bee Species

Amount of Species:

1.Sumatera Utara Tetragonula minangkabau, Sundatrigona moorei22.BantenTetragonula laeviceps

13.Jawa Bara tTetragonula laeviceps/

14.Jawa Tengah Tetragonula laeviceps 15.Kalimantan BaratHeterotrigona itama16.Kalimantan TimurHeterotrigona itama/ 17.Kalimantan SelatanHeterotrigona itama, Tetragonula laeviceps, Geniotrigona thorasica / 38.Sulawesi SelatanGeniotrigona insica, Lepidotrigona terminate / 29.Nusa Tenggara BaratTetragonula fuscobalteata110.MalukuTetragonula fuscobalteata 1The distribution of Trigona species are quite diverse.

Tetragonula laeviceps is the most widespread species, over four provinces: Banten, Jawa Barat, Jawa Tengah and Kalimantan Selatan. Tetragonula laeviceps tends to colonize in Java island, while Heterotrigona itama spreads over three provinces, namely Kalimantan Barat, Kalimantan Timur, and Kalimantan Selatan.

There are indications Heterotrigona itama is an endemic species in Kalimantan island. Tetragonula fuscobalteata species spreads across NTB and Maluku which are the eastern provinces of Indonesia. However, the other species found only in one province.

The resins composing the Trigona propolis are collected by the Trigona bee from various plants. We identified that there are at least 31 kind of plants as the source of the collected resin. Based on our observation, Trigona bee in Sulawesi Selatan is the species that has the highest propolis production.

Mango is the source plant with the highest resin contribution because it spreads over nine provinces, i.e., Sumatra Utara, Banten, Jawa Barat, Jawa Tengah, Kalimantan Timur, Kalimantan Selatan, Nusa Tenggara Barat, Sulawesi Selatan, and Maluku.

Jackfruit is the second source plant and spreads across eight provinces, i.e., Sumatera Utara, Banten, Jawa Barat, Jawa Tengah, Kalimantan Timur, Kalimantan Selatan, Nusa Tenggara Barat, and Maluku.

The other source plants are avocado, acacia, cempaka, jackfruit, cocoa, mahogany, and soursop.

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Beekeeping Eva Crane, in Encyclopedia of Insects (Second Edition), 2009 Stingless Bees (Meliponinae) in the Tropics

In the Old World tropics, much more honey could be obtained from honey bees than from stingless bees, and the latter were seldom used for beekeeping. But in the Americas, where there were no honey bees, hive beekeeping was developed especially with the stingless bee, Melipona beecheii, a fairly large species well suited for the purpose. It builds a horizontal nest with brood in the center and irregular cells at the extremities, where honey and pollen are stored.

The Maya people in the Yucatan Peninsula in Mexico still do much beekeeping with this bee. The hive is made from a hollowed wooden log, its ends being closed by a wooden or stone disk. To harvest honey, one of the disks is removed to provide access to honey cells; these are broken off with a blunt object, and a basket is placed underneath the opening to strain the honey into a receptacle below. Many similar stone disks from the 300s b.c. and later were excavated from Yucatan and from the island of Cozumel, suggesting that the practice existed in Mexico at least from that time.Nogueira-Neto in Brazil developed a more rational form of beekeeping with stingless bees.

In Australia, the native peoples did not do hive beekeeping with stingless bees, but this has recently been started.

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Nest Building Robert L. Jeanne, in Encyclopedia of Insects (Second Edition), 2009 Food Storage

Bumble bees construct specialized wax pots in which they store honey and pollen during periods of good foraging. Stingless bees and honey bees store pollen and enough honey to sustain the adult population through the unfavorable season.

The “honey wasps” (Brachygastra spp.) of the Neotropics also store large amounts of honey in their brood cells for the same purpose. Many other species of social wasps store enough honey as droplets in empty brood cells to get the colony through several days of poor foraging. Desert seed-harvester ants stockpile seeds in chambers in their nests, and honey ants (Myrmecocystus and others) store large amounts of honey in the crops of specialized workers called repletes. The fungus ants and higher termites in the subfamily Macrotermitinae (Termitidae) grow specialized fungus as food in chambers in their nests (Fig. 2).

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Purchase book Volume 2 Nathan Lo, ... Benjamin P. Oldroyd, in Encyclopedia of Animal Behavior (Second Edition), 2019

Stingless Bees of the Genus Melipona The first evidence for a genetically based mechanism of caste determination came from the Meliponini: a tribe of primarily monoandrous, stingless bees from tropical regions. Several species have been domesticated for honey production.

In the 1940s, Warwick Kerr noticed that in the genus Melipona, queens and workers are reared in identical cells, are fed identical food, weigh the same after emergence, and that queen pupae are scattered randomly through the brood comb (Kerr, 1950a).

This suggested that caste determination in Melipona was not determined by differential feeding or other environmental means.Kerr examined the brood of several Melipona marginata and M. quadrifasciata colonies and noticed that the ratio of queens to workers in the brood was ∼1:3 and 1:7 respectively.

He realized that these ratios could be explained by the segregation of two or three caste-determining genes, respectively. Kerr proposed that queens are heterozygous at all caste-determining loci, whereas workers are homozygous at one or more caste-determining loci as shown in Fig. 2.

Notice how all M. marginata queens are AaBb and will therefore produce four kinds of gametes at equal frequency from a simple Mendelian segregation: 1 AB: 1 Ab: 1 aB: 1 ab.

As with all other Hymenoptera, the Meliponini are haplo-diploid: the females are diploid, but the males are haploid and arise from unfertilized eggs. Therefore, males are produced by the doubly heterozygous M. marginata queens in this exact same genetic ratio.

This means that there are four kinds of males in the population. For each of the four kinds of males, 1/4 of their diploid female offspring will be queens because they can only mate with doubly heterozygous queens (Fig. 2).

Similarly, for M. quadrifasciata, and six other species, 1/8 of female progeny will be queens. Thus, the proportion of potential queens in the population is kept constant because of genic balance at the caste-determining loci.

The proportions of each allele are kept equal in the population: any rare allele is at a strong selective advantage because it is likely to be found in heterozygotes and thus passed on by queens, while any common allele is at a disadvantage as it is more likely to be present in homozygous workers and thus not passed on.

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Fig. 2. Model for caste determination in Melipona marginata.

Individuals that have at least one of two genes homozygous develop into workers, while those with both genes heterozygous (shaded) develop into queens.

What happens to all the extra queens? Melipona colonies are founded by swarms that contain large numbers of workers (as opposed to independent colony founding by queens) and there is only one single-mated queen per colony.

Thus, even with the three-locus system, where ‘only’ 1/8 of female brood becomes a queen, an excess of queens is produced. Queens emerge continuously, and whenever there is a laying queen in the colony, they are killed by the workers (Ratnieks, 2001).

Nonetheless, Melipona colonies have at least some capacity to reduce the number of queens produced when they are not required, for the number of queens produced declines in unfavorable seasons when food resources are scarce. Thus, there is a strong environmental component to the caste determination mechanism.

Melipona workers have five ventral nerve ganglia, whereas most queens have four, presumably because the two distal ganglia become fused at the pupal stage. Intriguingly, a small proportion of workers show the four ganglia typical of queens, and these were interpreted by Kerr as being genetic queens that had failed to develop phenotypically because of inadequate nutrition.

The quantity of food provided to the brood cells by nurse workers seems to be the determinant of whether a genetic queen can develop the full queen phenotype (Kerr, 1950a,b).

Melipona is the only genus of social bees that has equal-sized cells for workers and queens, and the only bees for which GCD has been proposed.

Perhaps the reduced ability of workers to influence the caste of larvae developing in sealed cells is the reason why the GCD mechanism has evolved in these bees. It should be noted that Kerr’s model has been questioned by some researchers, who suggest that a more complex model may be required.

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Regulation of Age Polyethism in Bees and Wasps by Juvenile Hormone Susan E. Fahrbach, in Advances in the Study of Behavior, 1997

C SUMMARY To summarize, the social bees and wasps provide numerous examples of age polyethism, ranging from strong expression in honey bees, some stingless bees, and the advanced social wasps to more variable expression in bumble bees and primitively eusocial wasps.

It is a testable hypothesis that all cases of strong age polyethism will be associated with high levels of juvenile hormone in individuals working outside the hive and in associated changes in the brain space devoted to the mushroom bodies.

Conversely, such changes in the structure of the adult nervous system are unlikely to be seen where age polyethism is weak and the youngest workers can both work in the nest and forage.

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Reduviid Predators Dunston P. Ambrose, A. Ganesh Kumar, in Ecofriendly Pest Management for Food Security, 2016

6 Reduviids as General Predators Because reduviids are generalist predators, they may attack beneficial arthropods and few reduviids appear to specialize on beneficial insects. For instance, stingless bees, Trigona (Jurine), are useful pollinators.

Several apiomerines wait for these bees at flowers or at sites where the bees visit to collect the resin for their nest construction and prey upon them.

They may smear the resin from the site on their forelegs to seize the prey. The kairomones of apiomerines also attract the bees (see in Pionar, 1992).

Fossil “resin bugs” and stingless bees have been found together in Dominican amber from at least 25 million years ago indicating their old relationship (see Ambrose, 2000a).

In India, Acanthaspis siva (Distant), preys upon the Indian honey bee, Apis indica F., and P. plagipennis on the other honey bees in their hives (McKeown, 1942; Ambrose, 2000a).

Another bug, Sycanus collaris (Fabricius) preys upon the tasar silkworm, Antheraea mylitta D. (David and Ramamurthy, 2011).

The role of “generalist” and “specialist” reduviid predators against insect pests needs to be studied. Some generalists may attack certain specialist predators, with potentially negative effects on pest control.

Hence, a proper assessment of role of reduviid predators in the regulation of insect pests in diverse crop systems and management of environment and habitat to increase reduviid predators need attention.

The reduviids are known to prey upon ladybird beetles in cotton fields and the generalist, Z. renardii (both nymphs and adults) preying upon lacewing, Chrysoperla carnea (Stephens), in cotton fields in the San Joaquin Valley (see Ambrose, 2000a).

Zelus renardii imposes heavy mortality (up to 10%) on C. carnea and thereby renders it ineffective as biocontrol agent. The decreased lacewing survival has been attributed to predation by reduviids than competition for aphid prey (Rosenheim and Wilhoit, 1993; Rosenheim et al., 1993; Cisenros and Rosenheim, 1997).

Zelus renardii not only influences the prevalence of intraguild predation but also the intensity of disruption of aphid biocontrol; while, none of their immature stages was found effective biocontrol agent of cotton aphid. Though such situation has not yet been recorded in India; a proper assessment of the role of reduviids predators in the regulation of insect pests in diverse crop systems and in the management of environment and habitat is necessary and important (Ambrose, 2002; Ravichandran, 2004; Nagarajan, 2010; Kumar, 2011; also see Ambrose, 1999, 2000a)."

https://www.sciencedirect.com/topics/agricultural-and-biological-sciences/stingless-bees

📷 This scientific research article is accessible here on ResearchGate!

Article Stingless bees (Meliponini): senses and behavior

Editorial Published: 12 August 2016 Stingless bees (Meliponini): senses and behavior Michael Hrncir, Stefan Jarau & Friedrich G. Barth Journal of Comparative Physiology A volume 202, pages597–601 (2016)Cite this article11k Accesses 29 Citations 13 Altmetric Metrics

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Abstract

Stingless bees (Hymenoptera, Apidae, Meliponini) are by far the largest group of eusocial bees on Earth. Due to the diversity of evolutionary responses to specific ecological challenges, the Meliponini are well suited for comparative studies of the various adaptations to the environment found in highly eusocial bees.

Of particular interest are the physiological mechanisms underlying the sophisticated cooperative and collective actions of entire colonies, which form the basis of the ecological success of the different bee species under the particular conditions prevailing in their respective environment.

The present Special Issue of the Journal of Comparative Physiology A provides a sample of the exciting diversity of sensorial and behavioral adaptations in stingless bees, particularly concerning

(1) the sensory bases for foraging,

(2) chemical communication, and

(3) the behavioral ecology of foraging.Stingless bees (Hymenoptera, Apidae, Meliponini) are by far the largest group of eusocial bees on Earth.

With more than 500 described species (Michener 2013), they outmatch the honey bees by a factor of 50 (Apidae, Apini: 11 species; Michener 2007) and even comprise twice the number of known bumble bee species (Apidae, Bombini: approximately 250 species; Michener 2007).

Their pantropical distribution, through the tropical America, Africa, Southeast Asia, and Australia (Fig. 1), suggests that the Meliponini had their origin on the ancient Gondwana continent more than 100 million years ago (Sakagami 1982; Camargo and Pedro 1992).

Today, the vast majority of stingless bee species is found in the Neotropics, where they represent a large taxonomic diversity (more than 400 nominate taxa in 32 existent genera) and an impressive variety of life histories (Camargo 2013).

Fig. 1📷Pantropical distribution (blue color) of stingless bees (Apidae, Meliponini). After Sakagami (1982)

Full size image

Despite their ecological importance, primarily as pollinators in most tropical ecosystems, knowledge about the biology of stingless bees is still rather moderate as compared to that about their celebrated relatives, the honey bees. This situation has, in part, historical reasons.

The first written references mentioning meliponine bees are due to Spanish and German explorers in Central and South America and arrived in Europe in the 16th century. They were followed by reports from Australia in the 17th century (Crane 1999; Engels 2009; Jones 2013).

These early accounts and subsequent archeological studies, particularly in the Mesoamerican region, revealed a long and rich tradition of meliponine honey hunting and well organized beekeeping dating back to at least 300 BC (Crane 1999). In Pre-Columbian Mayan societies stingless bees even were an essential component of mythology (Fig. 2) and the management of meliponine colonies (meliponiculture) was, and still is, a central issue of indigenous ceremonials (Crane 1999; Jones 2013).

More detailed studies on stingless bees by European explorers began only during the 19th century, at a time when scientific research on honey bees had already advanced for almost 200 years (Quintal and Roubik 2013).

In addition to the delayed attention received by science, the relatively low economic value of stingless bees as honey- and wax-producers, the often difficult access to their natural habitats, and the failure to maintain their colonies outside of the tropics, have all contributed to a scientific recognition that does not meet their relevance and interest.

Most importantly, the vast and rapidly growing body of both detailed and broad knowledge of the honey bees (particularly Apis mellifera) (Fig. 3) has often raised unjustified doubts about the relevance of investigating “just another group of eusocial bees”.

Fig. 2📷Source: http://www.famsi.org/mayawriting/codices

Stingless bees in Mayan mythology. Representations of the Mayan bee god Ah-Muzen-Cab (to the left of each panel, in yellow or orange color) together with other gods or god-like figures holding stingless bee hives and brood or storage pots (to the right). From pages 104 (left panel), 108 (middle panel), and 109 (right panel) of the Madrid Codex (c. 900–1521 AD).

Full size image

Fig. 3📷 Publications on highly eusocial bees (Apini and Meliponini) since 1945.

a Cumulative number of publications on honey bees (blue lines) and stingless bees (red lines).

b Proportion of articles on stingless bees relative to the total of publications on highly eusocial bees.

Publications registered in ISI Web of Science (solid lines) and Scopus Citation Database (dashed lines).

Search keywords: Apini/honeybee/honey bee/Apis/Apini/Apinae/Honigbiene; Meliponini/stingless bee/meliponine/Meliponina/meliponidae/sem ferrão/stachellos

Full size image

So, why shall we study stingless bees?

First, we need to get rid of the concept that stingless bees are nothing more than honey bees without a sting (or, as a matter of fact, with a vestigial and not functional sting; von Ihering 1886) and, therefore, essentially show the same physiological characteristics and behaviors.

In fact, the divergent evolution of the Meliponini and the Apini for more than 100 million years since the late Cretaceous (Cardinal et al. 2010) resulted in two very distinct bee groups.

Both the stingless bees and the honey bees are classified as highly eusocial (colonies with adults of two generations, castes and division of labor, cooperative work on brood cells, permanent colonies; Michener 1974).

Whereas the modern Apini constitute a small and morphologically, physiologically, and behaviorally uniform group (Michener 2007), the Meliponini evolved into a highly diverse tribe.

This applies to their

body size (ranging from species smaller than fruit flies to species larger than honey bees),

colony size (number of individuals ranging from a few dozens to several thousands),

nesting biology (subterranean nests;

non-arboreal or arboreal cavities;

association with termites, ants or wasps; exposed nests),

brood cell-arrangement (horizontal or, rarely, vertical combs; irregular clusters),

queen production (few queens in special brood cells;

multiple queens in unspecialized cells),

foraging strategy (solitary foraging; foraging in small or large groups; aggressive or unaggressive group foraging) and

underlying recruitment mechanism (vibratory activation of nestmates; goal-directed guidance of nestmates through pheromones),

and other still little explored traits (Michener 1974; Sakagami 1982; Johnson 1983; Wille 1983; Engels and Imperatriz-Fonseca 1990; Roubik 2006; Barth et al. 2008).

This rich diversity may be the result of accelerated speciation rates in the tropics owing to higher mutation rates, and/or faster physiological processes at higher ambient temperatures (Currie et al. 2004).

Moreover, the co-occurrence of several dozen of social bee species and their competition over common resources (food, nesting space, etc.) is believed to have resulted in the segregation of ecological niches and the obvious diversification of adaptive strategies (Roubik 1989; Biesmeijer and Slaa 2006).

Due to the diversity of their evolutionary responses to specific ecological challenges, the Meliponini are well suited for comparative studies of the various adaptations to the environment found in highly eusocial bees.

Of particular interest in this context are the physiological mechanisms underlying the sophisticated cooperative and collective actions of entire colonies, which form the basis of the ecological success of the different bee species under the particular conditions prevailing in their respective environment.

The present Special Issue of the Journal of Comparative Physiology A provides a sample of the exciting diversity of sensorial and behavioral adaptations in stingless bees, adding important information to recent publications on Meliponini differing in focus (scientific journals: Stingless bees: Biology and management, 2006, Apidologie 37/2; Stingless bees: Integrating basic biology and conservation, 2014, Sociobiology 61/4; books: Vit et al. 2013; Cortopassi-Laurino and Nogueira Neto 2016; Heard 2016).

The first part of the present Special Issue is dedicated to (1) “The sensory bases for foraging”. It compiles information about visual and olfactory mechanisms which enable Neotropical and Australian Meliponini to cope with the sensory challenges in different foraging environments.

When searching for food, visual cues are important for foragers to detect flowers from a distance.

Here, color preferences (both innate and modulated through previous experience), visual acuity, spatial resolution, and light sensitivity of the bees’ eyes are key physiological characteristics to identify flower patches in complex visual habitats, such as tropical rainforests (Dyer et al. 2016a, b; Koethe et al. 2016; Streinzer et al. 2016).

Once at the food source, foragers need to decide which flowers to visit and which to avoid. Footprints, left by previous visitors, are important chemical cues in this context because they indicate whether or not a flower still provides the desired resource.

The bees’ reaction to these scent marks (attraction, avoidance) is not innate; rather, foragers quickly learn their actual meaning in each new foraging context (Roselino et al. 2016).

A recently increasing anthropogenic menace concerning the sensorial and cognitive capacities of foraging bees is the indiscriminate use of agrochemicals.

Exposure to sub-lethal doses of pesticides, for example, compromises the neuronal plasticity of bees during ontogenesis.

This leads to a reduced brain volume, particularly of the mushroom bodies and optical lobes, in workers, therewith impairing their performance during foraging (Lima et al. 2016).

The second part of this Special Issue compiles information about (2) “Chemical communication”. Chemical communication signals are fundamental for coordinating collective actions of meliponine colonies, such as colony defense and food exploitation.

Mandibular gland pheromones released by workers, and also by males, when biting a potential nest-intruder trigger the collective attack of the enemy (Schorkopf 2016).

Chemical communication is also important to direct groups of foragers toward specific resources. Here, foraging strategies that rely on such goal-directed recruitment usually rely on pheromone marks at and near the exploited food patch. These conspicuous chemical signals are prone to eavesdropping and, thus, may attract competitors.

To avoid eavesdroppers, some meliponine species evolved alternative recruitment strategies, guiding large numbers of nestmates to food patches without using a scent trail (Flaig et al. 2016).

In the third part of our Special Issue, studies are presented that investigate the (3) “Behavioral ecology of foraging” in stingless bees.

To maximize the food intake into the nest, colonies need to fine-tune their foraging strategy according to the respective environmental situation, including climatic factors, presence or absence of competitors, identity of competitors, and resource abundance and quality.

Of these, climatic conditions, particularly air temperature and rain, constrain the foraging activity of a colony, yet affect different species differently. Thus, some species are able to collect resources under weather conditions that prohibit the activity of others, thereby avoiding interference competition at the food sources. In case that two or more species arrive simultaneously at a food patch, the presence of competitors, their aggressiveness and number might limit a colony’s access to this specific resource (Keppner and Jarau 2016). Here, a high abundance of food sources in the environment allows the colonies to switch to alternative patches, to collect more efficiently, and to return more quickly to the nest (Leonhardt et al. 2016). An elevated resource abundance and quality of food sources within the foraging area, moreover, stimulates the colonies to raise their foraging effort, therewith increasing the food intake rate into the nest (Schorkopf et al. 2016). Interestingly, and in strict contrast to honey bees, nest-internal food storage conditions influence the colony foraging activity of stingless bees only to a minor extent (Maia-Silva et al. 2016; Schorkopf et al. 2016). The difference between these two highly eusocial bee taxa is presumably due to differences in brood care (Apini: progressive larval feeding; Meliponini: mass-provisioning of brood cells), emphasizing the fundamental differences between stingless bees and honey bees concerning the proximate mechanisms that evolved to coordinate the observed colony behavior.Despite the steadily increasing number of scientific studies on stingless bees (Fig. 3), our knowledge about the Meliponini is still in the shadow of what we know from honey bees. In contrast to A. mellifera, which is considered an environmental generalist, many Meliponini occur in rather narrow geographic ranges (Camargo 2013), and are frequently restricted to a very specific habitat. Consequently, meliponine species often show a very strong association between their life history and a particular environmental situation. The study of stingless bees, therefore, will certainly help to reach more profound insights into how environmental factors shaped the physiological and behavioral mechanisms underlying the complex colony organization of highly eusocial bees. We very much hope that this special issue will stimulate future research on this fascinating and diverse group of eusocial bees, leading to a deeper understanding of meliponine neuroethology, as well as their sensory and behavioral physiology.References Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol A 194:313–327Article Google Scholar Biesmeijer JC, Slaa EJ (2006) The structure of eusocial bee assemblages in Brazil. 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Routledge, New YorkGoogle Scholar Currie DJ, Mittelbach GG, Cornell HV, Field R, Guégan JF, Hawkins BA, Kaufman DM, Kerr JT, Oberdorff T, O’Brien E, Turne JRG (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecol Lett 7:1121–1134Article Google Scholar Dyer AG, Boy-Genry S, Shrestha M, Lunau K, Garcia JE, Koethe S, Wong BBM (2016a) Innate colour preferences of the Australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol A. doi:10.1007/s00359-016-1101-4Google Scholar Dyer AG, Streinzer M, Garcia J (2016b) Flower detection and acuity of the Australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol A. doi:10.1007/s00359-016-1107-yGoogle Scholar Engels W (2009) The first record on Brazilian stingless bees published 450 years ago by Hans Staden. 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J Comp Physiol A. doi:10.1007/s00359-016-1110-3Google Scholar Maia-Silva C, Hrncir M, Imperatriz-Fonseca VL, Schorkopf DLP (2016) Stingless bees (Melipona subnitida) adjust brood production rather than foraging activity in response to changes in pollen stores. J Comp Physiol A. doi:10.1007/s00359-016-1095-yGoogle Scholar Michener CD (1974) The social behavior of the bees. Harvard University Press, CambridgeGoogle Scholar Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, BaltimoreGoogle Scholar Michener CD (2013) The Meliponini. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey: a legacy of stingless bees. Springer, New York, pp 3–17Chapter Google Scholar Quintal RB, Roubik DW (2013) Melipona bees in the scientific world: western cultural views. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey: a legacy of stingless bees. Springer, New York, pp 247–259Chapter Google Scholar Roselino AC, Rodrigues AV, Hrncir M (2016) Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context. J Comp Physiol A. doi:10.1007/s00359-016-1104-1Google Scholar Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New YorkBook Google Scholar Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143Article Google Scholar Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects, vol III. Academic Press, New York, pp 361–423Google Scholar Schorkopf DLP (2016) Male meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight. 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Francisco Mota 572, Mossoró-RN, 59625-900, BrazilMichael Hrncir Institute for Neurobiology, Ulm University, Helmholtzstrasse 10/1, 89081, Ulm, GermanyStefan Jarau Department for Neurobiology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090, Vienna, AustriaFriedrich G. BarthCorresponding author Correspondence to Michael Hrncir. Rights and permissions Reprints and Permissions About this article 📷Cite this article Hrncir, M., Jarau, S. & Barth, F.G. Stingless bees (Meliponini): senses and behavior. J Comp Physiol A 202, 597–601 (2016). https://doi.org/10.1007/s00359-016-1117-9Download citation Received 21 July 2016 Accepted 22 July 2016 Published 12 August 2016 Issue Date October 2016 DOIhttps://doi.org/10.1007/s00359-016-1117-9

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Springer Nature

© 2022 Springer Nature Switzerland AG. Part of Springer Nature."

https://link.springer.com/article/10.1007/s00359-016-1117-9

This article discusses stingless bees being developed in Australia as good pollinators:

https://beeaware.org.au/archive-news/stingless-bees-as-effective-pollinators/

"Stingless bees as effective pollinators"

📷

Stingless bee (Tetragonula carbonaria) foraging on citrus flowers. Photo: Dr Megan Halcroft

"Honeybees are excellent pollinators of many crops, but the burden placed on their health by pests and diseases is heavy. Added to that, the looming threat of a varroa mite incursion makes our reliance on honeybees for pollination decidedly risky.

In this context, the Hawkesbury Institute for the Environment at Western Sydney University is heading up the Hort Innovation project ‘Stingless bees as effective managed pollinators for Australian horticulture’.

The project’s overall objective is to investigate and develop potential alternative, native insect pollinators for use in horticultural crops. The leading candidates are stingless bees, because they can be managed in hives, just as honey bees are, and moved into crops as required.

Native stingless bees live in colonies and visit a variety of plants. They are currently used in macadamia crops, where their pollination services outperform honeybees.

The project has many parts, including the collection and review of data on the Australian stingless bee industry, with a particular focus on the current and potential use of stingless bees as managed pollinators.

The first stage of the project is to test whether the bees visit flowers and transport pollen within the crop. Studies will then be conducted to assess the bees’ impact on fruit and seed set, yield and quality. For the most promising crop and bee combinations, more detailed studies will be conducted to determine best ways to deploy managed hives within the target crop.

Lead researcher at the Hawkesbury Institute for the Environment, James Cook, said the research had the potential to change the way we view pollination in Australia. “It is already clear that managed stingless bees may have wide but underdeveloped potential for crop pollination,” he said.

“Stingless bees are also used in crop pollination in several Asian countries- such as India and Thailand – and there is good scope to exchange knowledge and expertise on bee biology, husbandry and deployment in horticulture.”

When Hort Innovation and Western Sydney University launched the project last December, Hort Innovation chief executive John Lloyd said the horticultural industry was keenly aware of the need to safeguard Australia’s food crops.

“To help do this, we need to consider alternative pollinators, investigate their performance in different crops, and find better ways to propagate and deploy them,” he said.

The project is currently seeking the participation of horticultural groups in a survey, with the aim of better understanding the needs of growers in terms of their crop’s pollination service requirements and management practices, such as pesticide use, which affect insect pollinators. The survey can be found on the Bees Business website.

This project is part of the Hort Frontiers Pollination Fund‘s ‘Supporting a healthy pollination future’ and aims to enhance and support existing pollinators, as well as identify the most effective pollination methods for various horticultural crop types.

Acknowledgement: Reproduced with permission from Dr Megan Halcroft. "

SOURCE LINK: https://beeaware.org.au/archive-news/stingless-bees-as-effective-pollinators/

Dear Sherwin Baja . See the following useful RG link: Article Options for stingless honey-beekeeping around Udzungwa Mount...

Kindly see also the following useful RG link: Article Diversity, local knowledge and use of stingless bees (Apidae...

Also check please the following useful RG link: Chapter From Extraction to Meliponiculture: A Case Study of the Mana...

The following RG links are also very useful:

Article Challenges and perspectives for beekeeping in Ethiopia. A review

https://www.sciencedirect.com/science/article/abs/pii/S002220112030063X

This article observes that the Global Community is slowly growing aware of the dangerous threat to the world food chain which is being caused by the depletion of the popular honey bees, which are well known pollinators. In view of the fact that there are tens of hundreds of other bee species descended from the same common ancestor in the kingdom of the bees. This is a scientific research article which tries to address this problem of the decline in the numbers of bees as pollinators which enable plant life, including life-giving forests, to thrive:

https://hal.archives-ouvertes.fr/hal-00892203/document

"Apidologie 37 (2006) 293–315 293
c INRA/DIB-AGIB/ EDP Sciences, 2006 DOI: 10.1051/apido:2006022 Review article Stingless bees in applied pollination: practice and perspectives Ester Judith Sa,b, Luis Alejandro S ´ Cb, Katia Sampaio M-Bc, Frouke Elisabeth Hd a Institute of Integrative and Comparative Biology and Centre for Biodiversity and Conservation, University of Leeds, LS2 9JT Leeds, UK b Centro de Investigaciones Apícolas Tropicales, Universidad Nacional, Costa Rica, Apartado postal 475-3000 Heredia, Costa Rica c Laboratório de Abelhas, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, n.321 CEP 05508-900 São Paulo, Brazil d Tropical Bee Research Unit, Behavioural Biology Department, Utrecht University, PO Box 80.086, 3508 TB Utrecht, The Netherlands Received 17 October 2005 – revised 27 February 2006 – accepted 28 February 2006

Abstract – At present, numbers of both wild and managed bee colonies are declining rapidly, causing global concern for pollination services.

Stingless bees play an important ecological role as pollinators of many wild plant species and seem good candidates for future alternatives in commercial pollination. This paper reviews the effectiveness of stingless bees as crop pollinators. Over the past six years the number of crops reported to be effectively pollinated by stingless bees has doubled, putting the total figure on 18 crops. Eleven stingless bee species across six genera have been found to forage effectively under enclosed conditions, indicating the potential of stingless bees as pollinators of greenhouse crops.

The biological features that make stingless bees strong candidates for commercial pollination services are discussed, together with their present limitations. The effects of natural vegetation and wild bees on crop yield are reviewed, and make a strong case for habitat conservation. agriculture / alternative pollinators / food crop / greenhouse / Meliponini

1. ECONOMIC IMPORTANCE OF POLLINATION IN COMMERCIALLY GROWN CROPS

Most crop plants depend on pollination for fruit and seed set. For many of these crops, insects are the main pollination vector (with the main exception of grains, which are windor self-pollinated).

It has been estimated that about 30% of human food is derived from bee-pollinated crops (O’Toole, 1993 cited in Kearns and Inouye, 1997). A wide variety of Corresponding author: E.J. Slaa, [email protected] bee species are known to be efficient and effective pollinators of many crops (e.g. Freitas and Paxton, 1998; Heard, 1999; Richards, 2001; Kremen et al., 2002).

Nevertheless, the European honeybee (Apis mellifera L.) is the single most commonly used species in managed pollination services, and the dependency of commercial crop yields on honeybee pollination is enormous everywhere.

The economic value of honeybees as agricultural pollinators has been estimated for several countries (e.g. ranging between $1.6 and $5.7 billion per year for the United States of America; Southwick and Southwick, 1992) and £137.8 million per year for selected crops in the United Kingdom (Carreck and Williams, 1998)), and far Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006022 294 E.J. Slaa et al. exceeds their economic value as producers of honey, wax and other hive products (Carreck and Williams, 1998).

On a global scale, the total annual value of agricultural pollination has been estimated at $200 billion (Kearns et al., 1998).

2. COMMERCIAL POLLINATORS

2.1. Why look for new species? Recently, numbers of both managed and wild bees are declining rapidly, causing global concern for pollination services (e.g. Watanabe, 1994; Buchmann and Nabhan, 1996; Kearns and Inouye, 1997; Nabhan et al., 1998; Cane and Tepedino, 2001; UNEP, 2002; Villanueva et al., 2005; see Ghazoul (2005a, b) and Steffan-Dewenter et al. (2005) for a discussion on this topic). Threats include habitat destruction or alteration, overuse of pesticides, parasites and diseases, and the introduction of alien species (Buchmann and Nabhan, 1996; Kearns and Inouye, 1997; Kremen et al., 2002).

Management of honeybee hives is handicapped worldwide by infectious diseases and parasites such as varroa mites (Varroa destructor), American Foul Brood, (Bacillus larvae), and Chalk brood (Ascosphaera apis) (Watanabe, 1994). In response to the worldwide decline of pollinator populations and pollinator diversity, the “Conference of the Parties to the Convention on Biological Diversity” established an International Initiative for the Conservation and Sustainable use of Pollinators in 2000. One of the main aims of this Initiative is to “promote the [...] sustainable use of pollinator diversity in agriculture and related ecosystems” (UNEP, 2002).

Diversification of crop pollinators would help to achieve pollination services when the commonly used pollinator (specifically honeybees for most crops nowadays) is not available in sufficient numbers. In addition, honeybees are not always the most efficient pollinators due to various factors, e.g. a miss-match in body size and flower size, low nectar production and specialized pollen release mechanisms in some plants, including those with poridical anthers (Kearns and Inouye, 1997).

When honeybees do not efficiently pollinate a given crop, it is probably economically beneficial to search for a better pollinator-plant match. It has been estimated that in the US alone, the commercial value of non-honeybee pollinators to crop yields may be as high as $6.7 billion per year (see Kearns et al., 1998).

Over the last several decades the management of some other pollinators has been developed which have proven to be much more efficient than the honeybee for certain crops. Examples include Nomia, Osmia, Megachile (for alfalfa), bumble bees (for crops of the Solanaceae family, e.g. tomatoes), flies, and more recently, stingless bees (Torchio, 1987; Free, 1993; Heard, 1999).

The best-known example is probably the success-story of the commercial use of bumble bees for the pollination of tomatoes (see Free, 1993). In tomato flowers, as a member of the Solanaceae family, pollen is released through vibration (‘buzzing’) of their poricidal anthers.

Bees produce these vibrations by shivering the indirect flight muscles, and anther buzzing has been observed in many bee species, including bumble bees and stingless bees of the genus Melipona. Not all bee genera however seem to show this behaviour; e.g. honeybees and stingless bees other than Melipona are not buzz-pollinators (Buchmann, 1983).

Greenhouse tomato flowers were commonly pollinated by hand using an electrical vibrator, but are now almost all successfully pollinated by commercially bred bumble bees (see Free, 1993). In the UK, the total value of bee pollination was estimated to exceed £200 million per annum, of which bumble bee pollination in green houses accounted for nearly 15% (£29.80 million) (Carreck and Williams, 1998).

A negative side to such a success story is the risk of establishment of exotic pollinators in non-native areas. Both bumble bees and solitary bees used for pollination services have been exported to different parts of the world to enhance crop pollination, and in many cases established successfully.

Introduction of exotic bee species causes general concern because of its potentially negative effects on both native pollinators and plants (see Goulson, 2003). Stingless bees in applied pollination 295 To avoid introduction of exotic flower visitors, some researchers have tested native bumble bee species for pollination services (see Kaftanoglu, 2000 (Turkey); Mah et al., 2000 (Korea)).

Besides physical properties hindering efficient pollination, honeybees may have other drawbacks in pollination services. First, honeybee colonies have seasonal cycles with a long inactive period in temperate regions which makes them less suitable for the pollination of off-season products.

Second, honeybees have a functional sting, and although the tendency to sting is quite low in several breeds of European honeybees, it may still cause problems for crop workers who are allergic.

In addition, all honeybees present nowadays in the Neotropics are Africanized (e.g. Caron, 2001; Schneider et al., 2004), which requires additional safety measures due to their aggressive nest defense (Winston, 1992). This is especially a problem in enclosed areas such as greenhouses, and in fields close to human or animal establishments.

An economic drawback to the commercial use of bumble bees is that colonies die after reproduction. New hives need to be bought repeatedly, making this pollinator service rather expensive, especially for small-scale farmers in developing countries.

2.2. Why stingless bees?

Good candidates for future alternatives in commercial pollination can be found in the diverse group of stingless bees (Meliponini) (Rindfleisch, 1980; Roubik, 1995b; Heard, 1999; Sommeijer and de Ruijter, 2000). Stingless bees comprise a highly diverse and abundant group of eusocial bees that inhabit the tropical and subtropical parts of the world. Stingless bees form perennial colonies from which they forage year-round.

Worldwide several hundred species exist, which differ significantly in colony size (from a few dozen to tens of thousands of individuals), body size (from 2 to 14 mm; compare to 12 mm for honeybees), and foraging strategy (some species recruit nestmates to high quality food sources, like honeybees, whereas others forage mainly individually, like bumble bees) (e.g. Roubik, 1992; Michener, 2000; Slaa, 2003; Slaa et al., 2003a; Biesmeijer and Slaa, 2004; Nieh, 2004).

These inter-specific differences allow for selection of the most appropriate stingless bee for a given crop species and crop breeding system (greenhouse, open field, etc.).

Commercial pollination with stingless bees has hardly been developed yet, and some observed potential problems include domestication, colony reproduction and mass rearing, which are discussed in more detail in the ‘general considerations’ section at the end of this paper.

Nevertheless, several biological features make stingless bees strong candidates for commercial pollination services, as outlined below. Stingless bees are true generalists, collecting nectar and pollen from a vast array of plants (Heithaus, 1979a, b; Roubik, 1989; Ramalho et al., 1990; Biesmeijer et al., 2005). A single species can collect floral rewards from up to 100 plant species on a yearly basis (Heithaus, 1979b; Cortopassi-Laurino, 1982).

Nevertheless, individuals tend to specialize on a single floral species for a certain amount of time, a behavioural trait commonly referred to as flower constancy (Slaa, 2003; Slaa et al., 2003b).

Flower constancy leads to assortative mating of the visited plants and therefore to more efficient pollination (e.g. Darwin, 1876; Thomson, 1983; Campbell and Motten, 1985).

Less pollen is wasted due to selective transfer within a species, and less non-specific pollen reaches the stigma, preventing pollen competition and stigma clogging (Waser, 1983). The fact that stingless bees are generalists at the colony level but specialists at the individual level makes them theoretically good pollinators. Indeed, stingless bees are considered important pollinators of the native flora in tropical and subtropical parts of the world, and they have been found to contribute to the pollination of many crops and wild plants (see Heard, 1999 for a review).

Several species of stingless bees have been domesticated for centuries, especially by the Maya people in Latin America (see Weaver and Weaver, 1981; Crane, 1983, 1992; Cortopassi-Laurino et al., 2006, this issue). Nowadays, a number of papers on the use of 296 E.J. Slaa et al. rational hive boxes for the keeping of stingless bees is available, and hive management is fairly straightforward for certain species (but see below).

Although stingless bees naturally only occur in the tropics and subtropics, they have also been successfully exported and maintained indoors in colder climates, using temperature controlled rooms and/or hives (e.g. Utrecht University, The Netherlands; Japan (Maeta et al., 1992; Amano et al., 2000; Amano, 2004, pers. comm.)).

Besides the fact that many species of stingless bees can be managed in hives, several other features make this group very adequate for pollination services.

First, colonies don’t die after reproducing, unlike Bombus, and colonies are naturally long-lived (Slaa, 2006). This makes it relatively easy to keep individual hives for long periods of time (up to 60 years: Murillo, 1984).

Second, they lack a functional sting, which makes them especially suitable for pollination of crops that are cultivated in inhabited areas and in enclosures such as cages and greenhouses. In Costa Rica, for example, many seed producing companies grow ornamental plants in large netted, insect proof, cages. They have a high demand for pollinators, but because all honeybees are Africanised, and hence more defensive, honeybees are hardly used for pollination in such enclosures. In such cases, stingless bees might provide a solution (see Slaa et al., 2000a, b; Sánchez et al., 2002).

Third, many stingless bee species have proven to forage well in enclosed areas (see Tabs. I and V), and under adequate climatological conditions they forage year-round. This makes them especially suitable for offseason production of crops in green houses. Most species of stingless bees have a foraging range smaller than that of the honeybee, which may enhance foraging efficiency in confined spaces (Visscher and Seeley, 1982; Seeley, 1985; Katayama, 1987; Kakutani et al., 1993).

Fourth, because most stingless bees cannot survive cold winters, there is little risk of invasion when importing stingless bees to temperate climates. Note however that some species do live where it occasionally freezes, and combined with global warming these species might become feral when introduced outside the tropics of Capricorn and Cancer. Furthermore, they suffer from fewer diseases, pests and parasites than the honeybee (Nogueira-Neto, 1997), which simplifies colony management. While not all species can be used for commercial pollination (e.g. obligate parasites of other stingless bees, species with restrictive nesting habitats, extremely defensive behavior or destructive use of flowers), several species are good candidates as commercial pollinators because they can easily be kept in hives, have sufficient numbers of workers per hive and are non-aggressive (Roubik, 1995b; Heard, 1999).

The diversity of the group indicates that they may be of use to pollinate a wide range of crops and ornamental plants.

3. CROPS POLLINATED BY STINGLESS BEES

The first detailed review on the role of stingless bees in crop pollination appeared in 1999 by Tim Heard. Heard (1999) reported that stingless bees are effective and important pollinators of nine crops, and that they contribute to pollination in ∼60 other species out of the ∼90 crop species they were found visiting. Over the past years, several new studies on stingless bee pollination appeared (Tab. I). After the review by Heard in 1999 there is a clear trend towards a more experimental approach using enclosures such as bags, cages and greenhouses (cases 13–17 Tab. I). In the sections below a summary of each crop is given, using both published and unpublished data. Only the studies that appeared after 1999 are included. For a review of previous studies see Heard (1999). 3.1.

Crops effectively pollinated by stingless bees Coffea sp., Rubiaceae

Coffee is one of the most economically important crops, but its pollination requirements are not well understood. The two most important species are C. arabica and C. canephora (Free, 1993; Roubik, 2002a). Stingless bees in applied pollination 297 Table I.

Crops effectively pollinated by stingless bees. Studies 1–12 report on pollination under field conditions, studies 13–18 report on pollination under enclosed conditions. Studies 1–9 are reviewed in Heard (1999). Scientific name Common name Stingless bee Reference Crops reported by Heard (1999) 1 Bixa orellana Annato Melipona melanoventer See Heard (1999) Melipona fuliginosa 2 Myrciaria dubia Camu-camu See Heard (1999) 3 Sechium edule Chayote Trigona corvina, See Heard (1999) Partamona cupira 4 Cocos nucifera Coconut See Heard (1999) 5 Averrhoa carambola Carambola Trigona thoracica See Heard (1999) 6 Macadamia intergrifolia Macadamia Trigona spp. See Heard (1999) 7 Mangifera indica Mango Trigona spp. See Heard (1999) 8 Poumora cecropiaefolia Mapati See Heard (1999) 9 Theobroma grandiflorum Cupuaçu Trigona lurida See Heard (1999) Studies reported after 1999 10 Coffea arabica Coffee Trigona (Lepidotrigona) Klein et al. (2003a) terminata 11 Coffea canephora Coffee Trigona (Lepidotrigona) Klein et al. (2003b) terminata 12 Persea americana Avocado Trigona nigra, Can-Alonso et al. (2005) Nannotrigona perilampoides Geotrigona acapulconis, Ish-Am et al. (1999) Trigona nigerrima, Partamona bilineata, Nannotrigona perilampoides, Scaptotrigona pectoralis, Trigona nigra, Scaptotrigona mexicana, Trigona fulviventris, Plebeia frontalis, 13 Fragaria × ananassa Strawberry Plebeia tobagoensis Asiko (2004); Lalama (2001) Trigona minangkabau Kakutani et al. (1993) Nannotrigona testaceicornis Maeta et al. (1992) Tetragonisca angustula Malagodi-Braga and Kleinert (2004) 14 Nephelium lappaceum Rambutan Scaptotrigona mexicana + Rabanales et al. Tetragonisca angustula (unpubl. data) 15 Capsicum annuum Sweet pepper Melipona favosa Meeuwsen (2000) Melipona subnitida Cruz et al. (2004) Trigona carbonaria Occhiuzzi (2000) Melipona favosa Meeuwsen (2000) 16 Lycopersicon esculentum Tomato Melipona quadrifasciata Santos et al. (2004a); Sarto et al. (2005) Nannotrigona perilampoides Cauich et al. (2004) 17 Cucumis sativus Cucumber Scaptotrigona aff. depilis, Santos et al. (2004b) Nannotrigona testaceicornis 18 Salvia farinacea Nannotrigona perilampoides, Slaa et al. (2000a, b) Tetragonisca angustula 298 E.J. Slaa et al.

Coffea arabica C. arabica is the most common coffee species and is cultivated throughout the tropics. Coffee flowers are very attractive to a wide array of insects including honeybees and stingless bees (Heard, 1999; Klein et al., 2003a). Although C. arabica is largely self-fertile, and a relatively large fruit set may be obtained without any pollinators, several studies indicate that bee pollination increases coffee production (Free, 1993).

Recently Roubik (2002a, b) found that in Panama bee pollination resulted in a higher fruit set and heavier mature fruits compared to bagged branches from which pollinators were excluded, and concluded that bees consistently controlled over 36% of the total coffee production.

Klein et al. (2003a) found that coffee fruit set in Indonesia was higher in areas with a high bee diversity (approximately 90% fruit set) compared to areas with a low diversity (approximately 60% fruit set), and concluded that bee diversity, not abundance, was important for pollination success. Using bagging experiments, they found that 15 bee species, including four Trigona species, contributed to the pollination of this shrub. However, pollination efficiency (fruit set after a single flower visit) varied among the species, with Trigona (Lepidotrigona) terminata being the most efficient stingless bee pollinator (80% fruit set).

As a group, the less abundant solitary bees were more efficient pollinators than the more abundant social bees (honeybees and stingless bees). Coffea canephora C. canephora is an important cash crop in many tropical countries (Willmer and Stone, 1989). Flowers are self-sterile and wind was long believed to be the main pollinating vector (see Free, 1993).

However, several studies have now indicated that insects do make a considerable contribution to its pollination, with the main visitors being bees (Willmer and Stone, 1989; Klein et al., 2003b, c). In Indonesia, fruit set increased with both abundance and diversity of flower visiting bees (from approximately 70% to 95% fruit set).

Honeybees, solitary bees and stingless bees were all effective pollinators of this shrub. As with C. arabica, pollination efficiency differed highly among the species, with Trigona (Lepidotrigona) terminata being the most efficient stingless bee pollinator (84% fruit set).

As a group, the less abundant solitary bees were more efficient than the more abundant social bees (Klein et al., 2003b). Avocado, Persea americana (Lauraceae) Avocado originated in Central America, where honeybees are not native.

Two recent studies have shown that stingless bees are frequent visitors and efficient pollinators of avocado flowers in Mexico (Ish-Am et al., 1999; Can-Alonso et al., 2005). Ish-Am et al. (1999) conducted their study mainly outside commercial orchards because the application of insecticides highly reduced insect populations in commercial orchards. Based on species abundance on the flowers, foraging behaviour, and number of pollen grains on the insect’s body zones that came in contact with the avocado stigma, they concluded that eight to 10 species of stingless bees were effective pollinators of avocado, together with the Mexican honey wasp. Can-Alonso et al. (2005), working in commercial orchards, found that A. mellifera and Trigona nigra carried comparable amounts of avocado pollen grains on their bodies, but that this number was significantly less on Nannotrigona perilampoides. They too concluded that native stingless bees are potentially efficient pollinators of this crop. Strawberry, Fragaria × ananassa (Rosaceae)

Most strawberry cultivars are hermaphrodite and self-fertile, but cultivars may vary highly in their degree of self-compatibility due to differences in spatial segregation of anthers and stigmata and temporal separation between anther maturation and stigma receptivity (Free, 1993; Zebrowska, 1998; Malagodi-Braga, 2002).

Strawberry flowers can be pollinated by a wide range of vectors, such as solitary bees, flies, and even wind (Free, 1993), although these are not (yet) used in commercial strawberry production.

Honeybees are often used in greenhouses in Japan and the UK, although they might not be the optimal pollinator for strawberries under greenhouse conditions (Katayama, 1987; Kakutani et al., 1993). McGregor (1976) reports that Stingless bees in applied pollination 299 100% 90% 80% 60% 70% 50% 40% 30% 20% 10% 0% control (n=197) Am (n=544) control (n=360) Pt (n=721) Species SQ 1st 2nd 3rd

Figure 1. Effect of bee pollination on strawberry quality.

Strawberry fruits were classified into four quality categories (categories derived from The Greenery International qualification for strawberry: SQ: super quality, perfect cone, fruit diameter > 27 mm; 1st: light deformation, fruit diameter > 22 mm; 2nd: some deformation, fruit diameter > 18 mm; 3rd: Industry, deformed, fruit diameter < 17 mm). Control: no bees, Am: Apis mellifera, Pt: Plebeia tobagoensis. After Lalama (2001). strawberry plants do not seem to be very attractive to honeybees, and colonies used for strawberry pollination in greenhouses in Japan decreased in population size (Kakutani et al., 1993).

However, in commercial strawberry fields in Brazil flowers yielded a lot of pollen and nectar and were abundantly visited by honeybees and stingless bees (MalagodiBraga, pers. obs.). Since the pollination studies in Japan (Kakutani et al., 1993; Maeta et al., 1992; see Heard, 1999), three more studies on strawberry pollination with stingless bees have appeared.

In The Netherlands imported Plebeia tobagoensis from Tobago, West-Indies, and honeybees were tested for their pollination effectiveness and efficiency under greenhouse conditions (each compartment 9 × 6 × 4 m, one colony for 100 plants; Hofstede, unpubl. data). When the bees were able to forage freely on the strawberry plants (var. Elan), honeybees had a significant positive effect on strawberry quality (Fig. 1, Mann-Whitney test, P < 0.005), and fruit quantity was somewhat higher (58% fruit set versus 48% without bees, Student-t test, F = 1.84, P = 0.063). P. tobagoensis had no effect on the number of fruits produced (74% versus 75% without bees, Mann-Whitney test, P = 0.8), but had a negative effect on strawberry quality (Fig. 1, Mann-Whitney test, P < 0.005). P. tobagoensis showed destructive pollen for100% 90% 80% 60% 70% 50% 40% 30% 20% 10% 0% 0 1 5 SQ 1st 2nd 3rd no fruits Am (n=48) Pt (n=109) Am (n=33) Pt (n=62) Am (n=141) Pt (n=74) # visits/flower Figure 2. Effect of controlled flower visits on strawberry quality.

Strawberry fruits were classified into four quality categories (categories derived from The Greenery International qualification for strawberry: SQ: super quality, perfect cone, fruit diameter > 27 mm; 1st: light deformation, fruit diameter > 22 mm; 2nd: some deformation, fruit diameter > 18 mm; 3rd: Industry, deformed, fruit diameter < 17 mm). Bees were allowed controlled visits to 2-day old flowers that were previously bagged to prevent destructive behaviour to the buds. Am: A. mellifera, Pt: P. tobagoensis. After Asiko, 2004. aging behaviour by entering closed flower buds (stigma not yet receptive) and biting the anthers (which haven’t released pollen yet) with their mandibles (Lalama, 2001). This behaviour could have been caused by the relatively low numbers of flowers available, but more observations are needed to confirm this. When buds were protected from the destructive behaviour through bagging before flower opening, P. tobagoensis did have a positive effect on strawberry quality (Fig. 2; Asiko, 2004). Five bee visits resulted in significantly higher quality fruits than no visits for both honeybees and stingless bees (Chi-squared test, P < 0.03, without significant differences between the two species (Chi-squared test, P = 0.7; Fig. 2). Fruit set tended to be higher after 5 bee visits than without visitation, but this was not significant (Chi-squared test, P = 0.14 for A. mellifera and P = 0.07 for P. tobagoensis; Fig. 2).

In Sao Paulo, Brazil, the only strawberry study site so far where stingless bees are native, five stingless bee species were initially tested for their suitability as strawberry pollinators in greenhouses (8 × 25 m): Nannotrigona testaceicornis, Tetragonisca angustula, Schwarziana quadripunctata, Scaptotrigona 300 E.J. Slaa et al. Table II. The effect of T. angustula pollination on strawberry (‘Sweet Charlie’ cultivar) production in greenhouses. Given are the mean±SD for various fruit measurements. Each greenhouse contained either one colony of T. angustula or no bee colonies (control). In the latter treatment the parcels were covered to prevent flower visitation by bees. After Malagodi-Braga, 2002. T. angustula control T-test Fruit number 490 ± 48 519 ± 84 NS % deformed fruit 6.9 ± 2.2 50.1 ± 12.9 t = 15.1, df = 40, P = 0.0001 Fruit weight (g) 9.6 ± 0.7 8.4 ± 1.2 t = 3.9, df = 40, P = 0.0003 bipunctata and Trigona spinipes (MalagodiBraga, 2002).

Two species, S. bipunctata and S. quadripunctata, did not forage under greenhouse conditions, and the other species showed a reduction in their daily foraging activity inside the greenhouse, despite resource availability and favourable values of air temperature and relative humidity.

Among all species T. angustula was remarkable for its relatively quick adaptation and the ability to keep satisfactory internal colony conditions (continuing cell construction and oviposition, maintaining their honey pots and storing pollen of strawberry flowers), even with frequent removals and introductions in greenhouses (Malagodi-Braga, 2002). T. angustula was tested for its pollination effectiveness using two different strawberry cultivars under greenhouse conditions.

Despite their small size (about 4.5 mm in length), T. angustula was found to be an effective pollinator of both the ‘Oso Grande’ cultivar (MalagodiBraga and Kleinert, 2004) and the ‘Sweet Charlie’ cultivar (Malagodi-Braga, 2002).

One colony, allowed to forage freely in a greenhouse with 1350 strawberry plants of the ‘Oso Grande’ cultivar, resulted in nearly 100% of primary flowers developing into marketable (well-shaped) fruits, compared to 88% for open pollination in the field, and 30%).

Visits to carrot and endive flowers resulted in a good seed set, which was not significantly lower than seed set after honeybee pollination, but significantly higher than seed set with T. angustula and the control (Tab. IV). During limited observations, bees only touched the stigmas consistently in carrot, endive and leek flowers.

Bees did not touch the stigmas of broccoli and rape flowers, and in only half of the visits did they touch the stigmas of chicory flowers. T. angustula visited only 4 of the 6 crops present, and preferred rape and leek flowers (> 30%). However, during visits to grape and leek flowers the stigma was never touched and those visits did not result in an increased seed set compared to the control (Tab. IV). T. angustula only touched the stigma of carrot flowers, but these flowers were hardly visited when other crops were available (Tab. III).

A. mellifera visited all crops but preferred endive flowers (Tab. III). Bees consistently touched the stigma in all crops, probably because of their larger body size, and increased seed set significantly compared to the control in 5 of the 7 crops.

Overall, A. mellifera was the most effective pollinator of the crops tested, followed by N. perilampoides.

Generally T. angustula Stingless bees in applied pollination 305 was the least effective pollinator, except for broccoli. N. perilampoides performed best as a pollinator of carrot and these flowers are relatively attractive to the bees. Although honeybees were at least equally effective pollinators for this crop, carrot flowers were not very attractive to honeybees (Tab. III), which may cause reduced visitation under field conditions when competing plants are nearby (Free, 1993).

4. GENERAL CONSIDERATIONS

4.1. Domestication To be able to use stingless bees for commercial pollination purposes, management of colonies in hives is of vital importance. Although many different species have been kept in hives (Cortopassi et al., 2006, this issue), not all species may be easily transferred to hives due to their specific nesting requirements (e.g. Geotrigona and Trigona fulviventris nest in the ground, Trigona corvina builds its own exposed nest, T. fuscipennis nests in termite nests). In addition, although they lack a functional sting several species aggressively defend their nest by biting or releasing a caustic substance, which makes them less suitable to manage in hives and for pollination services (e.g. the genus Oxytrigona and several species of the genus Trigona; see Biesmeijer and Slaa, 2004).

Although several species have been domesticated since ancient times (Cortopassi et al., 2006, this issue), management of stingless bee colonies is not as advanced as management of honeybee colonies (Cortopassi et al., 2006, this issue).

In addition, stingless bee management practices have been developed principally for the harvest of hive products, mainly honey.

Using colonies for commercial pollination services brings along different management requirements.

Colonies used for pollination services are much more disturbed than colonies used for honey production. Transportation to and from the crop, a limited diet offered by the crop (many crops offer no nectar), and less than optimal foraging conditions in greenhouses all put stress on the colony, often resulting in a loss of adult bees and a reduced brood production.

Some species may be better adapted to these stress factors than others, and some species may not forage at all under confined conditions (see Tab. V).

4.2. Mass rearing and colony reproduction Colonies used for pollination services need to be available in large numbers.

Nowadays stingless bee keeping is mainly a noncommercial small-scale business, although a few large-scale beekeepers exist in Mexico, Brazil, and Australia (Murillo, 1984; Heard and Dollin, 2000; Quezada-Euàan et al., 2001; Rosso et al., 2001; Drumond, 2004; Cortopassi et al., 2006, this issue) where it involves the keeping of mainly Melipona, T. angustula, Cephalotrigona and Scaptotrigona species.

In Australia, several beekeepers sell stingless bee hives (Trigona and Austroplebeia species), and they are listed on the Australian Native Bee Research Centre website (http://www.zeta.org.au/∼anbrc/buystingless-bees.html).

Some rent out stingless bee hives for pollination practices, mainly for pollination of macadamia (Heard and Dollin, 2000).

In Brazil, many farmers use stingless bees as pollinators of local crops, such as urucum, chuchu, camu-camu, carambola, cocoda-bahia and mango (Drumond, 2004).

Species that show aggressive nest defence also seem to exhibit intra-specific territorial behaviour, which makes them unsuitable for large-scale beekeeping where hives are placed close together (e.g. several Trigona species; Hubbell and Johnson, 1977; Wagner and Dollin, 1983).

One of the main problems for cultivating stingless bees at a large scale is that they naturally reproduce at a very low rate. It has been estimated that under natural conditions, colonies of most species reproduce only once every 20–25 years (Slaa, 2006), with the notable exception of a few common species such as the Neotropical T. angustula and the Asian Trigona minangkabau, that may reproduce up to once a year (Inoue et al., 1993; Slaa, 2006). 306 E.J. Slaa et al.

Table V. Stingless bee species that have been reported to forage under confined conditions and those that have been reported not to forage under confined conditions. Species Crop Foraging Greenhouse Location Reference size (l × w × h) Melipona favosa Sweet pepper Yes 9 × 6 × 4 m The Netherlands Meeuwsen (2000) M. quadrifasciata Tomato Yes 234 m2, 3 m high Brazil Santos et al. (2004a); Sarto et al. (2005) M. subnitida Sweet pepper Yes 83 m2 Brazil Cruz et al. (2004) Nannotrigona Tomato Yes 4 × 4 × 3.5 m Mexico Cauich et al. (2004) perilampoides Salvia farinacea Yes 6 × 3 × 3 m Costa Rica Slaa et al. (2000a, b) Salvia splendens No 6 × 3 × 2.5 m Costa Rica Bustamante (1998) Broccoli Yes 5 × 5 × 2 m The Netherlands Fonseca and Rape Picado (2000) Endive Chicory Leek Carrot N. testaceicornis Strawberry Yes 4.2 × 8.1 × 2.4 m Japan Maeta et al. (1992) Cucumber Yes 86.4 m2 Brazil Santos et al. (2004b) Plebeia Strawberry Yes 9 × 6 × 4 m The Netherlands Asiko (2004); tobagoensis Lalama (2001) Scaptotrigona Strawberry No 8 × 25 m Brazil Malagodi-Braga (2002) bipunctata Cucumber Yes 10 m high Japan Amano (2004) Eggplant Yes 10 m high Paprika Yes 10 m high Red pepper Yes 10 m high S.aff. depilis Cucumber Yes 86.4 m2 Brazil Santos et al. (2004b) S. mexicana Rambutan Yes 16 × 16 × 4 m Mexico Roubik pers. comm. S. quadripunctata Strawberry No 8 × 25 m Brazil Malagodi-Braga (2002) Tetragonisca S. farinacea Yes 6 × 3 × 3 m Costa Rica Slaa et al. (2000a, b); angustula Sánchez et al. (2002) Strawberry Yes 8 × 25 m Brazil Malagodi-Braga and Kleinert (2004) Rambutan Yes 16 × 16 × 4 m Mexico Roubik pers. comm. Broccoli Yes 5 × 5 × 2 m Fonseca and Picado Rape Yes The Netherlands (2000) Chicory Yes Leek Yes Radish Yes Meeuwsen (2000) Sweet pepper Yes Trigona White clover Yes 0.2 ha Japan Amano (2004) carbonaria Tomato Yes 0.2 ha Cucumber Yes 10 m high Eggplant Yes 10 m high Paprika Yes 10 m high Red pepper Yes 10 m high Sweet pepper Yes 3 × 5 × 4 m Australia Occhiuzzi (1999) T. fuscipennis S. splendens No 6 × 3 × 2.5 m Costa Rica Bustamante (1998) T. minangkabau Strawberry Yes 4.2 × 8.1 m Japan Kakutani et al. (1993)

Stingless bees in applied pollination 307 Colony management has been mainly focused on small-scale management practises (Cortopassi et al., 2006, this issue), where low colony reproduction rates have not been a major issue. Colonies can be artificially reproduced by dividing the hive population (adult bees and brood) in two parts, each part resulting in a new colony (e.g. Roubik, 1995b; Cortopassi-Laurino et al., 2006, this issue).

In the new colony lacking the mother queen, a virgin queen has to become accepted by the workers and has to mate outside with one or more drones, most likely from another colony.

This is no problem in their natural environment, where lots of drones are available, but becomes more problematic when colonies are exported to areas where they are not native.

Colonies of T. carbonaria have been split successfully in Japan, using a large greenhouse (10 m high) with multiple hives where ‘natural’ mating can take place (Amano, pers. comm.).

Nevertheless, records of successful mating or colony multiplication under enclosed conditions are scarce (but see Camargo, 1972; Cepeda Aponte, 1997; Amano, 2004).

So far, artificial insemination has not been developed for stingless bees but may be a valuable alternative to natural mating. Most people assume that under favourable conditions colonies can be multiplied about once a year. Even for the species that have been kept in hives since ancient times, the limiting factors for colony growth and colony reproduction are still mainly unknown.

More research is needed in this area before enough stingless bee colonies can be efficiently managed for commercial pollination purposes.

No major breeding populations exist yet outside the tropics. Further research could solve the current problem of artificial colony multiplication in non-native areas, although it might be economically more beneficial to restrict breeding to the tropical native areas and export existing colonies.

Keeping breeding programs in the tropics would also provide the opportunity for local people to benefit from their ecological resources.

4.3. Greenhouse pollination

Foraging under confined conditions (e.g. greenhouse, netted cage) brings along its own set of difficulties/complications.

One of the most common problems is foragers gathering in the top of the enclosure, especially during the first few days after introduction of the hive. These bees are a loss to the colony; when they manage to escape from the enclosure they do not come back, and if no escape is possible they often die of exhaustion and/or overheating (pers. obs.; Occhiuzzi, 1999; Amano, 2004). These bees are probably experienced foragers in search of a known food source.

Pilot experiments have shown that transportation of colonies over rough roads increases the incidence of orientation flights (Lukacs, pers. comm.), and it would be interesting to see whether (gentle) shaking of closed colonies before introduction in the greenhouse could reduce the problem of forager loss. However, shaking may also cause eggs, which float on top of the larval food, to drown, leading to mortality of young brood (Sommeijer, pers. comm.).

Although most stingless bee species that have been tried in pollination studies under confined conditions foraged effectively on the crop, some species were reported to not forage on the crop under confined conditions (Tab. V). This may suggest that some species are not suitable for greenhouse pollination. However, lack of foraging may also reflect suboptimal foraging conditions for the given species, such as a low attractiveness of the crop to the species, rather than a species-specific reluctance to forage under confined conditions. Clearly more studies are needed to get a better understanding of which factors attribute to successful foraging in greenhouses.

4.4. Pesticides

Application of pesticides is a common procedure in crop production, especially in the tropics where it still causes major health hazards for both people and animals.

Pesticide application to crops often repels insects from the flowers, can kill the pollinators and may 308 E.J. Slaa et al. Table VI. Mismatches between crop and stingless bee species. Crop Bee species Effective? Reference Salvia splendens T. angustula No, too small Sánchez et al. (2002) Strawberry P. tobagoensis No, pollen robbers Lalama (2001) P. tobagoensis Yes, if buds protected Asiko (2004) Tomato T. carbonaria No Amano (2004) Sweet pepper T. angustula No, does not touch stigma Kuyhor (2001) during nectar collection Radish T. angustula No, reaches nectary from outside corolla Thai (2001) kill entire colonies (e.g. Kearns and Inouye, 1997; Ish-Am et al., 1999; pers. obs.).

The chemical effect of commonly used pesticides on bees has been documented (see Roubik, 1995a), although most chemicals have only been tested on the honeybee.

Smaller-bodied stingless bees are probably even more susceptible than honeybees due to their high surface area-to-volume ratio.

During pesticide application managed hives can be removed from the site, but wild colonies may still be exposed to the chemicals.

Because colony reproduction rate of stingless bees is very low (see above), colony mortality will have a big impact on natural stingless bee populations.

There are several guidelines on pesticide application available to minimize the impact on pollinators, although none make pesticide use completely safe (Kearns and Inouye, 1997).

Biological control of pests, as is now offered in conjunction with commercially available bumble bee pollinators (e.g. Koppert BV, The Netherlands), seems an ideal solution.

However, special efforts to reduce the use of potent pesticides seem necessary in the tropics, where pesticides are easily available, generally cheap, and where safety risks are commonly unknown to the farmers.

4.5. Further research From the comparative studies described above it becomes clear that the pollination effectiveness of a specific stingless bee species depends very much on the crop species.

Table VI gives some examples of plant-pollinator mismatches from previous studies. A mismatch may result in visitation without pollination, stealing or robbing pollen and/or nectar. In some instances this can be prevented by evaluation of floral structure and relating the location of the stigma and anthers to bee body size.

Literature on techniques and considerations for pollination studies can be found in several other publications (e.g. Kearns and Inouye, 1993; Dafni et al., 2005). The effects of prolonged enclosed conditions and/or a restricted diet on colony health are largely unknown.

Regularly opening the hive to inspect the internal colony status, as often done in honeybees, is very disruptive for stingless bees, and often causes a decline in colony functioning.

Monitoring colony weight during pollination services can provide some insight into colony health, but does not provide information on brood status.

Recently, X-ray computerized tomography has been successfully used to visualize internal nest structures in a non-invasive way, and this method would provide an excellent research tool when measuring the effect of environmental (greenhouse) conditions on colony health (Greco et al., 2005).

5. POLLINATION AND BIODIVERSITY CONSERVATION

Although this manuscript deals mostly with the use of managed stingless bee colonies for pollination services, a fair share of pollination services can come from wild (unmanaged) bees.

For several crops it has been shown that growing crops near intact natural habitat (e.g. forest, woodland, chaparral) Stingless bees in applied pollination 309 increases abundance and diversity of flowervisiting insects, and that these crops have a higher yield than crops growing away from natural vegetation (Wille and Orozco, 1983; Venturieri et al., 1993; Heard and Exley, 1994; Kremen et al., 2002; Klein et al., 2003a, b; Ricketts, 2004; Ricketts et al., 2004; Chacoff and Aizen, 2006).

These findings indicate the importance of habitat conservation for pollination purposes.

Many wild bees, including stingless bees, depend on trees for nesting, and deforestation significantly reduces their numbers (Slaa, 2003).

Even selective logging may severely affect stingless bee populations, especially when the larger trees that are preferred for nesting are harvested (Eltz et al., 2002; Samejima et al., 2004).

In the case of coffee (C. arabica, see above), one of the most valuable export commodities from developing countries, yields on a farm in Costa Rica were 20% higher in areas near forest than in areas away from forests.

The economic value of the forest in terms of pollination services was estimated to be ca. $60 000 for one Costa Rican farm, per year. This value is of at least the same order as major competing land uses, which illustrates the economic benefit of forest conservation in agricultural landscapes (Ricketts et al., 2004).

Similar results were found in Indonesia where fruit set was negatively correlated with forest distance (Klein et al., 2003a), and in Brazil where coffee plantations near forest fragments had an increase of 15% in production that could be related to pollination services (Marco and Coelho, 2004).

Fruit set in the self-sterile lowland coffee species C. canephora was found to linearly decrease with distance from the forest (Klein et al., 2003b).

Proper information to farmers about the role of wild bees as pollinators and the pollination services of forests can play a major role in the conservation of wild bees and their natural nesting habitat of tropical forests.

Some species of stingless bees, especially from the genus Trigona, have dented mandibles and are known to damage fruits, leaves and sometimes even flower buds (Wille, 1961; pers. obs.).

Some farmers consider these species as pests and try to eliminate the easily recognizable exposed nests, without knowing that they are losing valuable pollinators.

Wille and Orozco (1983) report that one Costa Rican family with a chayote orchard took one year to eliminate all Trigona nests known in their area because they believed these bees ate the tendrils and young leaves.

After eliminating all nests, production decreased dramatically from previously high quantities of fruits to no yield at all.

Simple management measures to increase bee abundance and diversity include preservation of natural forests and forest fragments, increasing the availability of nesting sites, and minimizing the use of pesticides including herbicides (Kearns and Inouye, 1997; Klein et al., 2003b).

Conservation of stingless bees may also be affected by the commercial use of stingless bee colonies for pollination services.

Provided that colonies for such services are mainly obtained from breeding programs, instead of taken from nature, commercial use of stingless bees does not have to have a negative impact on the feral population, and may actually contribute to their conservation.

6. MAIN CONCLUSIONS AND PERSPECTIVES

This manuscript shows that stingless bees are effective pollinators of a wide range of crops.

Over the past six years, stingless bees have been confirmed as effective pollinators for nine new crop species, putting the total now on 18 crops.

Several species have been domesticated and can be managed in hives.

The main limitation to their commercial use as pollinators is lack of mass breeding techniques, which is hampered by low natural colony reproduction rates.

Stingless bees may be especially suitable to provide pollination services in greenhouses, as 11 out of the 13 species tested and reported foraged effectively under enclosed conditions.

However, more research is needed to find the optimal foraging conditions under enclosed conditions. Although feral colonies are restricted to the tropical and subtropical parts of the world, stingless bees can be kept in cold climates, where they have to be kept indoors in heated hives.

Stingless bees have successfully pollinated 310 E.J. Slaa et al. several greenhouse crops in regions with temperate climates, such as The Netherlands and Japan.

Pesticides may be a severe problem for stingless bees, as they are generally smallerbodied than the commonly used honeybees and bumble bees, but biological control could provide a good solution.

Although this paper has indicated some potential problems for the use of stingless bees in applied pollination, these can likely be overcome after more research.

Stingless bees possess several biological characteristics favourable in applied pollination, and this paper has further strengthened their importance as pollinators of commercially important crops.

This indicates that stingless bees are strong candidates in the search for alternative pollinators for our crops.

ACKNOWLEDGEMENTS

The authors would like to thank Tim Heard and David Roubik for valuable comments on the manuscript. Anne Dollin, Mark Greco, Darci de Oliveira Cruz, Manuel Rincon and David Roubik kindly provided some of the information presented in this paper.

Résumé – les abeilles sans aiguillon dans la pollinisation appliquée : pratiques et perspectives. Le nombre de colonies d’abeilles sauvages et élevées connaît actuellement un déclin rapide, provoquant une préoccupation mondiale quant aux services de pollinisation.

Les abeilles sans aiguillon (Apidae, Meliponini) sont des abeilles tropicales eusociales qui jouent un rôle écologique important comme pollinisateurs de nombreuses espèces de plantes sauvages.

Leur rôle comme pollinisateurs des cultures est actuellement étudié et plusieurs études ont été publiées ces dernières années depuis l’article de synthèse de Heard (1999).

Neuf cultures nouvelles ont été mentionnées comme étant efficacement pollinisées par les abeilles sans aiguillon, ce qui monte à 18 le nombre total de cultures en bénéficiant (Tab. I).

Cet article passe en revue les informations apparues depuis 1999 et inclut aussi bien des documents publiés que des données non publiées. Les études antérieures sont référencées dans l’article de Heard (1999).

Au cours des six dernières années les abeilles sans aiguillon ont été confirmées comme pollinisateurs du caféier (deux espèces), du fraisier (Figs. 1, 2 ; Tab. II), de l’avocatier, du rambutan, du paprika doux, de la tomate, du concombre et de la plante ornementale Salvia farinacea.

Il a été aussi reporté que les abeilles sans aiguillon visitaient et étaient des pollinisateurs potentiels de l’agrume calamondin, des cultures de cucurbitacées comme le melon d’eau et la citrouille, du radis et de plusieurs autres légumes tels que la carotte et l’endive (Tabs. II, IV).

Certaines espèces d’abeilles sans aiguillon diffèrent néanmoins grandement par leur taille et l’efficacité pollinisatrice dépendra de l’adéquation spécifique plante-pollinisateur (voir Tab. VI pour des cas où les deux partenaires sont mal assortis). La recherche récente s’est concentrée sur l’approche expérimentale à l’aide d’enceintes telles que sachets, cages et serres.

On a trouvé que onze espèces d’abeilles sans aiguillon représentant six genres butinaient efficacement sous enceintes (Tab. V), montrant ainsi le potentiel de ces abeilles comme pollinisateurs des cultures protégées.

Les colonies peuvent être maintenues à l’intérieur durant des années et, contrairement aux bourdons, ne meurent pas après la période de reproduction.

Ceci constitue une incitation économique pour utiliser ces abeilles sans aiguillon comme pollinisateurs commerciaux.

Dans les régions tempérées le fait que la plupart des espèces ne survivent pas aux climats froids, ce qui rend donc l’invasion des régions tempérées improbable, constitue une incitation économique.

Actuellement la principale limitation à leur usage commercial pour des services de pollinisation réside dans le manque de connaissances pour les élever en masse.

Il est nécessaire d’avancer dans la mise au point de la reproduction artificielle des colonies pour que les abeilles sans aiguillon puissent être disponibles comme pollinisateurs commerciaux.

Outre l’utilisation de colonies élevées dans des ruches, les abeilles sauvages de la végétation naturelle environnante peuvent fournir une bonne contribution aux services de pollinisation.

Il a été montré un accroissement de la production des cultures dans des plantations situées près de la forêt naturelle pour plusieurs cultures dont le café, qui est partiellement pollinisé par les abeilles sans aiguillon et représente l’une des cultures d’exportations les plus précieuses pour les pays en développement.

Ces résultats montrent l’importance économique de la préservation des habitats dans des buts de pollinisation commerciale. Apidae / Meliponini / abeille sans aiguillon / pollinisateur / culture protégée / culture alimentaire Zusammenfassung – Stachellose Bienen in der angewandten Pollinisation: Praxis und Perspektiven.

Die Zahlen an wilden und beimkerten Bienenvölkern gehen derzeit rapide zurück, was zu einer weltweiten Bedrohung der Bestäuberdienste führt.

Die Diversifizierung der kommerziell verfügbaren Bestäuber kann eine der Antworten sein, um die Lebensmittelproduktion in der Zukunft zu Stingless bees in applied pollination 311 garantieren.

Stachellose Bienen sind tropische eusoziale Bienen, die eine wichtige Rolle als Bestäuber vieler Wildpflanzen spielen. Ihre Rolle als Bestäuber in der Landwirtschaft wird erst seit kurzem untersucht, und seit dem letzten Übersichtsartikel von Heard (1999) wurden viele neue Arbeiten erstellt und publiziert.

Neun neue Feldfrüchte konnten durch Stachellose Bienen effektiv bestäubt werden. Dies bringt ihre Gesamtzahl nun auf 18 (Tab. I).

Die vorliegende Arbeit stellt die nach 1999 erschienenen Informationen über Stachellose Bienen als Bestäuber in der Landwirtschaft zusammen, und zwar sowohl aus publizierten als auch aus unveröffentlichten Dokumenten.

Ältere Studien sind in dem Übersichtsartikel von Heard (1999) berücksichtigt. Während der letzten sechs Jahre konnten Stachellose Bienen als Bestäuber von Kaffee, Erdberen (Abb. 1 und 2, Tab. II), Avocado, Rambutan, Gemüsepaprika, Tomate, Gurke und Salvia farinacea, einer Zierpflanze, etabliert werden.

Ausserdem werden Stachellose Bienen als Besucher und potentielle Bestäuber von Calamodin, Cucurbitaceen, wie z.B. Wassermelone und Kürbis, für Rettich und verschiedene andere Gemüse wie Karotte und Endivie beschrieben.

Stachellose Bienen weisen jedoch erhebliche Artunterschiede hinsichtlich ihrer Körpergrösse auf, und die Bestäubungeseffizienz wird davon abhängen wie gut die Bestäuber- und Pflanzenspezies zusammenpassen (siehe Tab. VI für einige Misserfolge).

Neuere Untersuchungen zielen auf experimentelle Ansätze in geschlossenen Systemen, wie Taschen, Käfigen und Gewächshäusern. Elf Arten Stachelloser Bienen aus sechs Gattungen erwiesen sich in solch geschlossenen Systemen als effektive Sammlerinnen (Tab. V), was auf ein beachtliches Potential Stachelloser Bienen als Bestäuber in Gewächshäusern hindeutet.

Von wirtschaflicher Bedeutung für die Nutzung Stachelloser Bienen als Bestäuber dürfte die Tatsache sein, dass ihre Kolonien über Jahre hinweg in geschlossenen Räumen gehalten werden können und dass, im Unterschied zu Hummeln, diese Kolonien nach dem Reproduktionsvorgang nicht eingehen.

Von ökologischem Interesse für ihren Einsatz in gemässigten Klimaten ist, dass die meisten Arten nicht kälteresistent sind, was die Gefahr der Invasion und Ausbreitung in diesen Gebieten unwahrscheinlich macht.

Das momentan grösste Problem für die kommerzielle Nutzung Stachelloser Bienen für Bestäuberdienste sind die mangelnden Kenntnisse für ihre Massenaufzucht. Die künstliche Reproduktion von Kolonien muss weiterentwickelt werden, bevor sie als kommerzielle Bestäuber in Frage kommen.

Ausser der Nutzung bearbeiterter Völker können auch wilde Kolonien aus der umgebenden natürlichen Vegetation einen wichtigen Anteil an den Bestäuberdiensten erfüllen. Eine gesteigerte Produktivität in nahe an Naturwäldern gelegenen Plantagen konnte für verschiedene Fruchtpflanzen gezeigt werden, einschliesslich Kaffee, der (teilweise) von Stachellosen Bienen bestäubt wird und der ein wertvolles Exportprodukt in Entwicklungsländern darstellt.

Diese Befunde zeigen die Bedeutung der Habitatkonservierung für kommerzielle Bestäubungszwecke. Landwirtschaft / Bestäuberalternativen / Feldfrüchte / Gewächshaus / Apidae / Meliponini

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In Puglia there are some beekeepers, but studies like the one you describe do not seem to me to be in progress.