Colony Function and Communication

  • José Javier G. Quezada-Euán


Workers of M. beecheii performing different activities in the brood area.


Age polyethism Juvenile hormone Ecdysteroids Task allocation Task partition Life span Specialization Caste Subcaste Food transference Waste management POP Trophic egg Cleptobiosis Soldier Suicidal bite Aggressive response Resin Lactobacilli Immune system Hygienic behavior Semiochemical Scent mark Trail pheromone Cuticular hydrocarbon Nestmate recognition Food communication 

Workers of M. beecheii performing different activities in the brood area.

How colonies work as a coherent unit is one fascinating aspect of insect societies. The mechanisms that these small organisms, with apparently limited capacity for reasoning and decision, use to produce sophisticated responses (highly structured nests, comb construction, food gathering, and colony defense), cooperating as a functional unit, have captured the scientific interest for centuries. Today, it is generally accepted that social coordination seems based on individual behavior, and that communication and information among colony members are key aspects to produce coordinated responses (Seeley 1995).

In social insects, there is no central control of the activities; no individual or group of individuals decide which tasks are performed, nor who, when, where, and how they are performed (Seeley 1998). The large number of individuals conforming colonies would make this type of control inefficient, due to the time it may require for the information to flow up to one central control and back to the executers (Gordon 2016). Rather, it seems that workers react with individual responses to diverse stimuli, which in turn affect the behavior of nearby nestmates. Individual responses are somehow integrated to build group level organized and a coordinated behaviors (Page Jr. 2013). Organization relies to a great extent on the ability to learn and the capacity to communicate among colony members (Biesmeijer 1997). The latter, the capacity to communicate, is especially relevant as it allows passing on and receiving information among nestmates, from which coordinated actions result (Seeley 1995).

Surprisingly, not much is yet known about colony integration in Meliponini compared with the honey bees (Seeley 1995; Biesmeijer 1997). However, accumulating evidences are allowing a better understanding on how colonies work and the proximate mechanisms involved in communication. This chapter covers some general aspects of the organization of work in stingless bees, with descriptions of particular behaviors, like the process of oviposition and the mechanisms of defense. In the last two sections, I summarized information of chemical and physical communication in Meliponini.

5.1 Organization of Activities

Stingless bee societies are formed by three types of individual, males, queens (reproductive females), and workers (partially sterile females). The workers are by far the main body of colonies; in stingless bees their numbers range from a few hundred to over tens of thousands depending on the species (Sakagami 1982). Workers perform most activities, including the construction of different structures, feeding of the larvae and the queen, as well as defense of the nest, and collection of food and other materials.

Similar to the honey bee, the various tasks that stingless bee workers perform across their life can be roughly divided in activities inside and outside the colony. There is also an intermediate phase in which the workers perform guarding and orientation flights before they dedicate to external activities (Michener 1974). However, how the progression across tasks and task assignment are achieved is a complex phenomenon that is still not well understood. Like in the honey bee, the progression of worker stingless bees across different tasks is strongly related to age and is known as age polyethism (Wilson 1971). Interestingly, age polyethism is flexible, meaning that workers can progress or revert across different activities, depending on the needs of their colonies (Robinson and Huang 1998). Artificial manipulation of colonies has shown that if young workers are eliminated, foragers can revert to performing nest activities despite their older age (Sommeijer 1987).

Although stingless bee workers transit through a series of activities, these and the age at which they perform them depend on the status of individuals (threshold to different stimuli), colony needs, and changes in the environment (Biesmeijer 1997). The status of individuals depend on physiological changes related to age. Titers of morphogenetic hormones like ecdysteroids, and Juvenile Hormone (JH) vary with worker age and seem to affect individual sensibility to perform different tasks. In the honey bee, it has been shown that such hormones play basic roles in the transition of workers across different activities (Hartfelder et al. 2002; Robinson and Huang 1998; Page Jr. 2013). However, in stingless bees the interaction between the different hormones show important differences with the honey bees (Hartfelder et al. 2006). In some species, like M. quadrifasciata, the levels of JH and ecdysteroids show low hemolymph titers during the first days after emergence in both, workers and queens, which is similar to what occurs in the honey bee (Hartfelder et al. 2002). Nonetheless, in species like M. scutellaris, JH titers are highest in nurse bees decreasing markedly in foragers (Cardoso-Júnior et al. 2017a). A reverse situation is found in worker honey bees, in which JH titers constantly increase as workers age (Hartfelder et al. 2002; Page Jr. 2013). These findings suggest that stingless bees may have maintained the ancestral gonadotropic function for JH (Cardoso-Júnior et al. 2017a). Also in contrast with honey bees in which vitellogenin titers peak in young workers, stingless bees’ vitellogenin patterns do not show marked relationship with worker age (Hartfelder et al. 2006).

There is also a genetic component of polyethism and some bees tend to perform certain activities more frequently than others; some may not even perform certain activities at all (Biesmeijer 1997). Recently, findings in M. scutellaris suggest a possible mechanism linking genotype component with larval diet and activity (Cardoso-Júnior et al. 2017b). It seems that differences in global methylation of the genome in the larval-pupal stages favor the activation of genes related to task allocation in the adult bee (Cardoso-Júnior et al. 2017b).

As explained before, flexibility in task performance is one important characteristic of polyethism in the highly eusocial bees. Due to this particularity, the term work division or division of labor, which suggests a rigid system of task performance, may be better changed to task allocation (Gordon 2016). The term task allocation includes elements of plasticity, suggesting that the assignment of individuals to different tasks could vary in response to the constantly changing stimuli in the environment and individual thresholds, determined physiologically and genetically (Gordon 2016).

Externally, workers of the highly eusocial bees are remarkably uniform (but see Grüter et al. 2012), in comparison with ants or termites, in which highly differentiated worker morphologies exist (Wilson 1971). Thus, in highly social bees, the term caste seems more appropriate for the two morphologically and physiologically different individuals of the female sex, the workers, and the queen (Michener 1974). The subdivision that exists among workers of the highly eusocial bees regarding allocation to different activities may be better referred to as subcaste.

In general, the activities performed by the workers in the highly social bees could be organized along two main principles (Ratnieks and Anderson 1999; Hart and Ratnieks 2001):
  • Task allocation : Workers are assigned to major groups of tasks like nursing, defending, or foraging.

  • Task partition: The main tasks are divided among groups of workers, usually of different age, in different subtasks. For instance, nectar collection is more efficiently performed by two groups of workers, foragers and receivers. Interestingly, task partitioning seems exclusive of highly eusocial species, being absent in the Bombinini and Euglossini (Hart and Ratnieks 2002).

Generally, the activities performed by stingless bee workers fall into five major groups (Sakagami 1982; Wille 1983):
  1. (a)

    Cleaning and reparing the brood chamber

  2. (b)

    Construction of cells and provisioning

  3. (c)

    Nectar reception and processing

  4. (d)


  5. (e)

    Nectar, pollen, and resin collection

Similar to honey bees, the first tasks occur in the nest and are performed by younger bees. As bees age, they start performing activities closer to the exterior. In M. beecheii, a detailed account on the activities of several workers, revealed a general pattern from “indoor to outdoor” performance as workers age. Nonetheless, a great deal of variation between individuals on the time and frequency dedicated to different tasks was also noted (Medina-Medina et al. 2014; Fig. 5.1). Young bees mainly engage in cleaning and construction in the brood area; they also have well-developed wax glands. Workers between 10 and 18 days produce trophic eggs, receive nectar from foragers, and spend a great deal of time in dehydrating it. Older bees (25–35 days) usually perform activities related with guarding and cleaning; they also start short-range flights presumably for orientation. After 35 days, workers start foraging.
Fig. 5.1

A general sequence of activities during the life cycle of a M. beecheii worker: (a) Construction and cleaning; (b) larval food provisioning and production of trophic eggs; (c) nectar reception and processing; (d) guard, orientation flights; (e) foraging

The average life span calculated for workers of M. beecheii was 52 days, with a range between 35 and 60 days (Medina-Medina et al. 2014; Fig. 5.1).

Some distinctive tasks and behaviors only found in stingless bees (Sakagami 1982; Wille 1983) are:
  1. 1.

    The collection of large amounts of resin

  2. 2.

    Mass provisioning of larval food

  3. 3.

    Excretion inside the nest, which probably delays engaging in external activities

  4. 4.

    The production of trophic eggs to feed the queen


The type of activity affects worker longevity, possibly due to the physical wear involved. In Costa Rica, Biesmeijer and Toth (1998) found that M. beecheii nectar foragers are more active and live on average 3 days. In contrast, pollen foragers are only active 1–3 h daily, and can live up to 12 days.

An interesting feature of task allocation in eusocial bees is specialization in field bees (Kolmes 1985). In stingless bees, some individuals prefer collecting nectar over pollen and vice versa (Biesmeijer and Toth 1998). In A. mellifera, it has been documented that nectar foragers also specialize on some kinds of flowers (Seeley 1995). It seems that task specialization is beneficial for the colony, increasing individual efficiency and performance.

In Melipona specialization on the collection of certain resource type seems less common; most workers indistinctively engage in nectar, pollen, or resin foraging, compared with honey bees (Biesmeijer and Toth 1998). Perhaps the small number of workers per colony in Melipona can explain why specialization on particular resources may not be adaptive. Non-specialized workers may more ready shift to collecting different resources as they are available.

The causes of specialization are not well understood. In A. mellifera some physical characteristics of the workers could affect their preference for collecting nectar or pollen. Forager honey bees were compared morphologically, and although no substantial differences in body size were found, pollen collectors had significantly more olfactory sensilla plates on the antennae compared with nectar collectors (Riveros and Groenenberg (2010).

In M. beecheii, Quezada-Euán et al. (2015) compared the body size of bees bringing nectar, pollen, and resin to the colony. Similar to the honey bee, body size did not vary between bees collecting different resources. Although the level of specialization of each worker was not determined, these results suggest that in the highly eusocial honey bees and stingless bees, body size does not seem crucial in determining specialization (Quezada-Euán et al. 2015). It is possible that the elaborate mechanisms of communication for food collection in the highly eusocial honey bees and Melipona (Winston 1987; Nieh et al. 2003) could restrain large size differences between individuals. Large size differences could produce “distortion” in the interpretation of messages related to distance and/or direction to food sources (Waddington 1989; see section 5.6). It would be interesting to verify if similar principles apply in non-Melipona species with less sophisticated communication systems (Jarau 2009) and that present significant body size differences between workers (Quezada-Euán et al. 2011).

One activity in which Worker body size seems important is guarding. Indeed, in some meliponine species, a guard subcaste has been identified, larger compared to other workers in the colony (Grüter et al. 2012, 2017).

In addition to the possible effect of morphological traits on specialization, there also seems to be an influence of experience and learning. In Pb. emerina workers specialize in the collection of resins only after a period of handling these materials which occurs after the second week of life (dos Santos et al. 2010).

One important aspect in stingless bees is that males engage in some activities (nectar dehydration, wax production) at least sporadically (Van Veen et al. 1997; Velthuis et al. 2005). In this regard males of stingless bees are more similar to workers (morphologically and behaviorally), compared to drones in the honey bee (Hartfelder et al. 2006; Medina et al. 2016).

The evidence to date suggests that work allocation shares some common features between stingless bees and honey bees but also important contrasts. It is possible that similarities in the general mechanisms (genetic and physiologic) behind age polyethism exist in both groups of bees (Robinson and Huang 1998; Hartfelder et al. 2006). However, it is important to note that substantial differences exist in the mechanisms controlling task allocation between both types of bee. Much work is still needed to better understand the organization of work and its proximate causes in the stingless bees.

5.2 Task Partitioning

For efficiency, one major task can be divided into subtasks, usually performed by workers of different age (Hart and Ratnieks 2002).

One activity in which partitioning has been studied in detail is the collection of food. In Apis nectar gatherers transfer nectar loads to receivers inside the colony, who store it in the combs; foragers do not discharge the nectar they bring into the cells (Hart and Ratnieks 2001). This type of partitioning increases efficiency and also provides feedback between field and hive bees during nectar collection (Seeley 1985).

Nectar transference between nectar collectors and receivers has been documented for various species of stingless bees: M. favosa (Sommeijer 1984), M.panamica (Nieh and Roubik 1998), and Ttgn. carbonaria (Nieh et al. 1999/2000). In a study in Yucatan, Hart and Ratnieks (2002) evaluated the rate of food transference in four species of stingless bee with different systems of recruitment, from primitive (N. perilampoides) to more developed (M. beecheii) (Nieh et al. 1999/2000; Schmidt et al. 2008). It was found that all species exhibited task partitioning during nectar collection. However, there were substantial differences in the rates of transference between collectors and receivers. In M. beecheii nectar collectors transferred loads to a larger number of receivers (up to 12). In Fr. nigra, Pb. frontalis, and Scp. pectoralis, with presumably less developed communication systems, nectar was transferred to less receivers (\( \overline{x} \)= 1.8). Interestingly, the lowest number of transferences was observed in N. perilampoides (\( \overline{x} \)= 1.5), which has a comparatively more primitive communication system. These results indicate that although task partitioning during food collection seems a common feature in stingless bees, there are differences in the intensity of interactions among workers, seemingly related to the sophistication of communication of food resources (Hart and Ratnieks 2002).

Surprisingly, M. beecheii foragers transferred food to a much larger number of receivers (\( \overline{x} \)= 5.7), even compared with A. mellifera, in which average transference from foragers to receivers is between 1.9 and 2.7 times (Kirchner and Lindauer 1994; Hart and Ratnieks 2001). Such a high rate of nectar transference in Melipona could be related to the more sophisticated communication system in this genus (Lindauer and Kerr 1960; Nieh and Roubik 1995, 1998; Nieh 1998), possibly involving some mechanism of food recruiting in addition to nectar processing alone. By sharing a load with multiple receivers, foragers may stimulate recruiting of more food collectors. On the other hand, a large number of food discharges could indicate that receivers may also be selective and refuse the nectar carried by some foragers, or that the demand for nectar has decreased. Nevertheless, in the honey bee nectar collection is largely determined by the number of receivers, rather than demand, that seems constant (Seeley 1985).

Another example of task partitioning in stingless bees is the management of waste. In most stingless bees, waste dumps are temporarily built in some areas of the nest. In M. beecheii, some workers engage in gathering waste pellets, Interestingly, they usually transfer such pellets (93% of cases) to other workers, who take them out of the nest (Medina-Medina et al. 2014).

The results on food collection and waste management in stingless bees, show that task partitioning seems to be exclusive to highly eusocial bees, albeit with various degrees of complexity across species. Interestingly, it seems that task partition has only evolved in species that found colonies through swarming, and is absent in species whose colonies are founded by individual females (Hart and Ratnieks 2002).

5.3 Food Provisioning and Oviposition Process

One of the most studied behaviors in stingless bees is the process of food provisioning and oviposition. The process of food provisioning of brood cells and the subsequent oviposition by the queen is a highly ritualized conduct showing diverse degrees of interaction and antagonism between queen and workers (Fig. 5.2.).
Fig. 5.2

Phases of the process of provisioning and oviposition (POP) in M. beecheii: (a) Final phase of cell construction with a “collared” cell. (b) The queen approaches the cell and stands on one side while the workers take turns to discharge larval food; the queen frequently taps them on the thorax with her front legs. (c) The queen inspects the cell occasionally, possibly ingesting some food. (d) After consuming the trophic egg or eggs laid by workers, the queen lays her egg. (e) The queen moves away. (f) One worker climbs on top and rotates while capping the cell with the cerumen collar

Sakagami and Zucchi (1966) studied the complex sequence of behaviors known as provisioning and oviposition process (POP). They divided the process in four general phases which also take place in Apis, but in a different order:
  1. 1.

    Cell construction (C)

  2. 2.

    Oviposition (O)

  3. 3.

    Provisioning of the larval food (P)

  4. 4.

    Cell closing (CC)


In honey bees the completion of the four phases takes roughly 8 days, because of the prolonged feeding of the larvae in open cells. The order, thus, is C-O-P-CC. In stingless bees, the whole process may only take 2 h and the sequence is C-P-O-CC. A distinctive characteristic of the process in stingless bees is the ritualized interaction between queen and workers between C and P.

Although the basic phases of the POP are similar across different stingless bee species (Sakagami 1982; Drumond et al. 2000), there is a great deal of variation in the duration of the different phases, aggression between queen and workers, number of cells oviposited, etc. Such interspecific variation has been subject of various phylogenetic analyses (Zucchi 1993; Drumond et al. 2000).

One possible explanation for the complex queen-worker interaction during the POP is that through ritualized behaviors, the queen reaffirms her reproductive dominance over the workers. This may be so because in Meliponini the queen’s chemical control of the workers seems generally less developed compared to the honey bee (Wille 1983; Zucchi 1993). Nonetheless, recent evidence indicates that chemical control of worker reproduction may occur in some species (Friesella schrottkyi) by means of queen cuticular compounds (Nunes et al. 2014a). Although stingless bees differ from honey bees in which the queen’s signal is mostly produced in the mandibular glands (Nunes et al. 2014a), these findings indicate that physical and chemical control of worker reproduction by the queen may be found at different degrees in stingless bees, and that both strategies may not be excluding.

The general process of the POP in M. beecheii is presented in Fig. 5.2. In this species the whole process from construction, to cell capping, takes around 14.9 min. Cell capping alone may take up to 8 min (van Veen 2000; Avila et al. 2005). The highest frequency of POPs in M. beecheii occur at night. During the day, the frequency of POPs is one approximately every 2 h, but in the evening they may occur every hour (van Veen 2000).

During the POP , in most species of stingless bee, the workers produce a type of egg as food for the queen. These eggs, known as trophic eggs, lack nuclei and are infertile (Koedam et al. 1996). Trophic eggs are also found in other insects in which they are used to feed the offspring (Crespi 1992; Perry and Roitberg 2006). Stingless bees are in this sense a rare exception in the insect world, because trophic eggs are used to feed the queen. Thus, trophic eggs seem to play an important, but little understood, part in the interactions between workers and queen during the POP (Sakagami 1982).

A characteristic of trophic eggs is an apparently incipient stage of development, compared with fertile eggs. The chorion is thinner and more fragile. It is believed that under the influence of the queen, trophic eggs are rapidly released from the worker’s ovaries, and thus, they cannot complete their development (Cruz-Landim 2000). In contrast, workers also produce fertile functional eggs and these have a thick chorion with a reticular pattern, similar to that of the queen’s (Koedam et al. 1996; Velthuis 1997). Chemically, there are differences in the surface of trophic and functional eggs too. In Melipona the queen’s eggs are rich in hydrocarbons C21–C29 which may help in repelling water, in combination with a reticular surface. In contrast, trophic eggs with little disturbance can easily sink into the larval food (Jungnickel et al. 2001).

Trophic eggs are found in almost all neotropical stingless bees, but the site where they are deposited during the POP varies across species (Sakagami 1982).

Trophic eggs in most Melipona species, are laid on top of the larval food or attached to the wall inside the cell (Fig. 5.3); in other stingless bees, eggs are more frequently laid on the rim of the cell (Sakagami 1982; Wille 1983).
Fig. 5.3

Worker (O, trophic) and queen (R) eggs in M. beecheii. The image underneath shows the position of both types of egg on the larval food

In several species of Melipona, trophic eggs are smaller than the queen’s (Aparecido-Pereira et al. 2006). However, in M. beecheii trophic eggs are relatively large and of similar size to the queen’s (Fig. 5.3). Curiously, eggs produced by the queen of different Melipona can have different shapes, but the size tends to remain constant across species, in spite of differences in body size of the adult workers (Velthuis et al. 2003).

An important difference in the POP of different species of stingless bees is the number of cells that are built, provisioned, and oviposited by the queen (Roubik 1989). In accordance to the number of cells and their location during the oviposition, different POP patterns have been identified:
  1. 1.

    Successive: In this pattern, the queen lays an egg in one cell which is sealed before the process starts in another cell. A few cells can be provisioned with larval food simultaneously (Melipona, Frieseomelitta). (Figs. 5.2 and 5.4).

  2. 2.

    Synchronic: A number of cells, up to a couple dozen, are simultaneously provisioned; when they are ready, the queen lays eggs in rapid succession (Nannotrigona, Plebeia). A few cells may be simultaneously capped by the workers, not one by one, as in the successive pattern.

  3. 3.

    Semi-synchronic: On the same comb there may be a few cells that are oviposited successively, while others are oviposited in synchrony, like in Scaptotrigona (Fig. 5.5).

  4. 4.

    Composite: The queen can lay eggs in two different combs, while the cells on one comb are provisioned and oviposited in succession, in other combs the provision and oviposition may occur in synchrony (Lestrimelitta) (Fig. 5.6).

Fig. 5.4

Successive mode of cell provisioning and oviposition in M. beecheii. A few cells are built simultaneously but only one is provisioned and oviposited after each POP (third from left to right)

Fig. 5.5

Semi-synchronic cell provisioning in S. pectoralis. On the same comb, a group of cells have been provisioned and are ready to be oviposited, while another group of cells are simultaneously built. The queen lays eggs consecutively in the cells that are ready

Fig. 5.6

Composite cell provisioning in L. niitkib. On each of two combs, more than a dozen cells are being built and provisioned simultaneously. The queen may lay eggs in the cells on one comb synchronically and successively, before moving to the other

5.4 Defense

In accordance to Hermann (1984), social insects face four principal classes of natural enemies: arthropod predators, vertebrate predators, insect parasitoids, and parasites and pathogens. One distinctive feature of highly eusocial insects is the build up of large reserves of food, representing a valuable source of energy and protein for other animals. Not surprisingly, together with the increase of reserves, the potential attraction of various types of robbers and predators increased as well (Breed et al. 2012). To avoid the potential risk of plunder, social insects have developed a series of strategies to protect their nests.

Because stingless bees can accumulate large amounts of honey and pollen, it is puzzling that this group of bees lost the functionality of the sting, one weapon commonly used by other social Hymenoptera for the protection of their nests. Nonetheless, these insects have evolved a series of seemingly equally efficient strategies to defend their nests (Kerr and Lello 1962; Grüter et al. 2012; Nunes et al. 2014a), which will be revised in this section.

It is not clear why stingless bees lost the functionality of their sting. However, it seems that the sting in bees is generally under-relaxed selection, allowing a wide range of morphologies and even gross reduction. Indeed, sting function has been lost in members of three more bee families apart from the Apidae (stingless bees); these are the Stenotritidae, Andrenidae, and Megachilidae (Packer 2003).

Some of the first stingless bees were small, and it is likely that they followed a defense strategy based more on crypsis and retreat (Wille 1979). Modern minute stingless bees still follow this type of strategy, they are timid (Kerr and Lello 1962; Wille 1979). In the course of time, the value of the sting as a defense mechanism in shy and inconspicuous species, may have been limited.

In A. mellifera, it is believed that the sting and venom evolved to defend the nest against large predators, mainly mammals (Winston 1987). Interestingly, the sting of the workers of A. mellifera has barbs and a ganglion associated, which keeps it buried in the skin while venom is pumped (Dade 1985). Another evidence of the use of the sting of A. mellifera against large predators is the presence of hyaluronidase and phospholipase in the venom. These two enzymes dilute the connective material of the skin making it easy for the other materials to disperse. Melittin and other compounds are responsible for the swelling and pain (Choo et al. 2010; Daneels et al. 2015). However, the production of venom is costly, as well as the massive attacks involved in defending the nest against large predators.

Presently army ants, cleptobiotic bees (Lestrimelitta), and frequently conspecific colonies are the main predators of stingless bees (Gloag et al. 2008; Grüter et al. 2016). It is likely that the sting and venom resulted gradually less useful against such attackers (Gloag et al. 2008; Grüter et al. 2016). Against other insects a tactic to immobilize the enemy or prevent invasion of the nest would be more advantageous (Shackleton et al. 2015). Attacking also represents high costs for the colony and a better strategy in species with low populations as many stingless bees, would be withdrawal and camouflaging. However, presently, there seem to be two main strategies of defense in stingless bees; one is crypsis and retreat, but in other speciesaggressive responses are the norm. In a few outstanding cases ( Oxytrigona ), defense also involves the use of chemical weapons (Wille 1979). Nonetheless, mass attacks seem to occur with more frequency in species with populous colonies.

As mentioned before, army ants and other meliponines are probably the main predators of stingless bee colonies today. Different strategies have evolved to defend against these attackers. In the case of army ants, stingless bees make use of resin to block their entrance or repel the attacks.

A major threat to stingless bees is pillage by colonies of the same or different species. Like other eusocial insects, stingless bees engage in robbing if the opportunity arises, and some species are particularly prone to it (Grüter et al. 2016). However, there are two genera of stingless bees that have specialized in stealing food and materials from other nests, a behavior known as cleptobiosis (Breed et al. 2012). Bees of the neotropical Lestrimelitta with approximately two dozen species (Camargo and Pedro 2007) and the African Cleptotrigona, with one species (Eardley 2004), are obligate cleptobionts. Workers of both species have lost the corbiculae and plumose hairs involved in the collection of pollen, and obtain food and building materials exclusively from robbing other stingless bees (Fig. 5.9). Lestrimelitta and Cleptotrigona are not phylogenetically related, indicating that cleptobiosis evolved independently in two different continents (Eardley 2004).

The attacks of cleptobiotic Lestrimelitta seem to be of particular importance in having shaped the defense strategies of stingless bees, most notably the evolution of morphologically distinct worker soldiers in some species. Worker polymorphism is rare in flying social insects (Grüter et al. 2017), although it is common in ants and termites (Hölldobler and Wilson 1990). It is argued that the evolution of morphological subcastes would be difficult in wasps and bees because of the limitations posed by flight (Waddington 1989; Quezada-Euán et al. 2013). Therefore, the pressure that cleptobionts exert on stingless bee colonies must be considerable for the evolution of such differentiated groups of workers. Apparently, a soldier subcaste has evolved more frequently in species that are preferred targets of Lestrimelitta (Grüter et al. 2012, 2017). Nonetheless, soldiers have been found only in species that defend aggressively by fighting cleptobionts. Species that are preferred hosts of Lestrimelitta but that do not fight (Sakagami et al. 1993) may not have guard subcastes, but this has not been evaluated.

Biting is a frequent strategy used by stingless bee workers to defend their nests. The mandibles are mainly used in the collection and handling of food and nest materials. However, the size and sharpness of the mandibles seem to have evolved in relation to the defensive capacity and aggressive behavior of different species (Shackleton et al. 2015). Biting in stingless bees frequently involve a suicidal behavior. During the defense, workers bite a target and do not dislodge their mandibles, even when the head is sectioned from the body (Shackleton et al. 2015) (Fig. 5.7).
Fig. 5.7

Worker of Scp. pectoralis biting. Biting is probably the most important defense strategy in stingless bees, and has a suicidal component

In species from Yucatan, the mandibles of the workers have remarkably different size and shape (Fig. 5.8). In two of the most defensive species, Scp. pectoralis and Pt. bilineata, a marked development in sharpness and relative size of mandibular teeth is evident. It is noticeable that large mandibles with sharp teeth are also present in M. beecheii (Fig. 5.8), compared with Brazilian species of Melipona, which lack sharp teeth (Shackleton et al. 2015).
Fig. 5.8

External surface of the right mandible of workers of various species of stingless bees in Yucatan. The teeth are located on the left margin and the curvature on the superior margin of the mandible, respectively

The mandibles of L. niitkib only have a couple small teeth, but a large blunt surface and reduced curvature on the inner margin are evident (Fig. 5.8). This type of mandible is probably designed to cause severe injuries when biting. Cleptobionts use force to raid some species and their mandibles may be specially designed to overcome their hosts’ aggressions. However, robber bees also use chemicals during raids, especially citral produced in their mandibular glands. Whether the shape of their mandibles is related to the use of chemical substances is unknown (Sakagami et al. 1993; Quezada-Euán et al. 2013). Aggression is not frequent in species with small workers, like N. perilampoides and Plebeia; instead they retreat when attacked. During the attacks of cleptobiotic bees, workers of these species cluster in circles with their heads inwards, probably to protect against the bites of robbers (Fig. 5.9). Perhaps this apparently defeatist behavior is important to avoid unnecessary deaths against a stronger enemy (Sakagami et al. 1993).
Fig. 5.9

Above: Intraspecific mass attack between colonies of L. niitkib. Below: Workers of Fr. nigra clustering with their heads inwards during an attack by L. niitkib

The intensity of the aggressive response of Yucatecan stingless bees falls into two main categories, intense or timid (Table 5.1). Intraspecific variation in the aggressive response is also evident (pers. Obs.). In M. beecheii, some colonies are aggressive and some are tame, but it is not known if differences in the aggressive response are linked to environmental variables or genetic components. In A. mellifera it is known that environmental (colony size, amount of food reserves, environmental temperature, and humidity), but also genetic factors affect the intensity of the aggressive response of colonies (Winston 1987).
Table 5.1

Defensive strategies of some species of stingless bees from Yucatán


Intensity of defense

Worker populationa

Strategy against mammals

Strategy against insects

Melipona beecheii



Bite, pheromone

Block nest entrance, suicidal bite

Scaptotrigona pectoralis



Massive attack, bite, recruit more attackers

Suicidal bite

Nannotrigona perilampoides




Resin to immobilize intruders, retreat





Resin to immobilize intruders, retreat

Frieseomelitta nigra




Block entrance, resin to immobilize intruders, retreat

Trigona fuscipennis



Massive attack, caustic bite, recruit more attackers

Suicidal bite, resins

Partamona bilineata



Massive attack, bite

Suicidal bite, resins

Trigona fulviventris




Block entrance, resins

Cephalotrigona zexmeniae




Block entrance, resins

Lestrimelitta niitkib




Suicidal bite

aFrom Quezada-Euán and González-Acereto 2002

Guarding and defense are among the final activities performed by workers (Sommeijer 1984). The risk involved in guarding and external activities is higher compared with nest activities. In this regard, the loss of workers of an advanced age would be less detrimental to colonies than losing young ones. In fact, older workers have a comparatively shorter life span and have already made a significant contribution to colony fitness (Tofilski 2002).

Stingless bees are avid collectors of resins and use them in the construction, but also during the defense of their colonies. Indeed, resin use can be considered a primary line of defense, in probably all stingless bee species (Leonhardt and Blüthgen 2009). Some species, like Fr. nigra, maintain large reserves of resin near the entrance and if an intruder breaks in, guards immobilize it, while others deposit drops of resin on legs and wings to bury it. This mechanism called mummification has been reported in various species of stingless bees, and is considered a defense strategy against large intruders that cannot be easily removed from the colony. Resin also protects the colony from bacteria and other microorganisms that may grow on corpses (Greco et al. 2010).

Stingless bees are frequently in contact with resin, enriching their cuticular chemical profile (Leonhardt et al. 2015). It has been suggested that resins compounds on the cuticle could be used as protection against microorganisms (Simone-Finstrom and Spivak 2010). Nonetheless, experimental manipulation of Asian stingless bees in which resin compounds were removed from the cuticle, were not more susceptible to fungus infections compared with bees kept intact (Leonhardt et al. 2015). However, resins were effective repellents against ants. Workers with large amounts of resin-derived compounds on their bodies were significantly less attractive to those predators (Leonhardt et al. 2015). Perhaps this may explain why resin collection increases when ant attacks become more frequent (Leonhardt and Blüthgen 2009). Resins can also be used as chemical mediators in inter- and intraspecific coexistence. It has been discovered that chemical compounds in the resins moderate aggression in coexisting Asian species (Leonhardt et al. 2010a).

Although resins may not be involved in the defense of stingless bees against disease, they may be important in the protection of a valuable resource, their food reserves. Stingless bees can store large food reserves which under tropical conditions may be easily spoiled (Roubik 1989). Some resin compounds incorporated in the cerumen of food pots could regulate the growth of microorganisms that may spoil pollen or nectar (Roubik 1989). On the other hand, some bacteria and yeasts may be beneficial for preserving the stored food. Perhaps stingless bees select different resins in accordance to antimicrobial properties, explaining why they are choosy when collecting them. Workers learn to collect resin from specific plants, and even slight variations of the plant’s chemical profiles can deter collection (Leonhardt et al. 2010b).

Bees, like other insects, are protected against disease by humoral and cellular components of their immune system . Surprisingly, evidence of a reduced individual immune response has been found in social insects, compared with solitary species (López-Uribe et al. 2016). In the honey bee, there is evidence that fewer genes related with the immune response are generally active, compared with solitary bees (Evans et al. 2006). It is argued that social insects may rely more on collective mechanisms, such as hygienic behavior, than on individual immune function to reduce the risk of disease (López-Uribe et al. 2016).

Social bees have also developed an association with certain microbes (microbionts) to protect against pathogens and to preserve food (Morais et al. 2013; Leonhardt and Kaltenpoth 2014; Kwong et al. 2017). Among the important bacteria living in stingless bees colonies are lactobacillus (Bacillus) important for the digestion of pollen. The lactobacilli soften the hard pollen exine and may produce antibiotics or lactic acid to protect food reserves from the invasion by other microorganisms (Menezes et al. 2013).

Some lactobacilli also inhabit the bee’s digestive system, and my be important probiotics for the prevention of disease (Vásquez et al. 2012). These microbes can be found in the gut just a few hours after the bee emerges (Vásquez et al. 2012). This suggests that Lactobacillus firms of highly social species seem transmitted both, horizontally (among individuals in the same generation), and vertically (between generations) (McFrederick et al. 2013). The association between corbiculate bees and gut microbiota seems an old one. At least five core gut bacterial lineages may have been acquired early in the evolution of eusocial corbiculate bees, possibly 80 million years ago (Kwong et al. 2017). Interestingly, lactobacilli species seem common across corbiculate taxa, with only a few firms restricted to particular hosts (McFrederick et al. 2013). For instance, L. kunkeei can be found in the digestive tract of M. beecheii and in the honey bee (Vásquez et al. 2012). In contrast, Leonhardt and Kaltenpoth (2014) identified some  Lactobacillus firms only in Australian stingless bees.

Some bacteria living in the colonies of stingless bees may protect against pathogens. For instance, Streptomyces, found in Trigona colonies from Brazil, produces antibiotics with inhibitory effect on the pathogens causing American and European foulbrood in the honey bee (Menezes et al. 2013). However, direct effects of this and other bacterium in disease protection have not yet been found in stingless bees.

Some stingless bees have reached impressive symbiosis with their microbiota . For instance, the larvae of Brazilian Scp. depilis feed on a fungus (genus Monascus) that grows on the liquid food and its elimination triggers larval mortality (Menezes et al. 2015). Similarly, Bacillus meliponotrophicus found in Trigona and Melipona may be involved in some unknown process vital for the colonies. The application of antibiotics/streptomycin to kill the bacterium resulted in their collapse (Machado 1971; Morais et al. 2013).

Microorganisms in the pollen and honey of stingless bees are important for fermentation and predigestion, but may also control spoiling bacteria and yeast (Morais et al. 2013). For instance, dehydration of pollen reserves in Ptilotrigona mediated by the yeast Candida protects them from decay (Camargo et al. 1992). It is known that some stingless bees (Trigona and Partamona) actively collect fungal spores, but the use in colonies has not been studied (Morais et al. 2013).

Although a large variety of microorganisms are associated with stingless bees, many aspects of their ecology and effect on the well-being of individuals, and colonies, have just started to be explored and understood (Morais et al. 2013).

As mentioned before, social bees seem to largely depend on collective behavioral mechanisms to fight disease. One of these mechanisms is hygienic behavior. The ability to detect and remove dead or contaminated brood and adults from nests has been known for over 50 years in the honey bee (Rothenbuhler 1964). In A. mellifera, hygienic behavior is performed by workers between 15 and 20 days old, before they start foraging (Spivak and Downey 1998). Hygienic bees use olfactory signals to detect diseased or dead brood, which they uncap and remove from the colony. Although hygienic behavior has a genetic component in the honey bee, the frequency of colonies expressing it is low, in the range of 10%. (Lapidge et al. 2002; Bigio et al. 2013).

Given its economic importance, hygienic behavior had been extensively studied in the honey bee (Rothenbuhler 1964; Spivak and Downey 1998). However, it was not known if the rarity of disease in stingless bees may be due by similar mechanisms. Medina-Medina et al. (2009) and Nunes-Silva et al. (2009) investigated if Meliponini may also use hygienic behavior for colony immunity. Medina-Medina et al. (2009) worked with two species of stingless bee from Yucatan (M. beecheii and Scp. pectoralis), while Nunes-Silva et al. (2009) investigated the Brazilian Pb. remota. In both studies a protocol similar to that used in A. mellifera to assess hygienic behavior (Spivak and Downey 1998) was applied. Sections of comb with dead pupae were introduced in test colonies and the number and time in which dead individuals were removed were registered. Interestingly, all three species of stingless bees exhibited hygienic behavior, but there were inter- and intraspecific differences in the number of pupae removed after 48 h, and the time to remove them completely from the combs. The most hygienic species were Pb. remota and Scp. pectoralis, with 96% and 66% dead pupae removed in 48 h, respectively. In comparison, M. beecheii colonies only removed between 30 and 40% dead pupae in the same period of time. In addition, it took M. beecheii 9 days to remove all dead pupae, while Scp. pectoralis accomplished that in just 3 days. It was also evident that intraspecific differences in hygienic behavior existed, suggesting this trait may have a genetic component in stingless bees. Recently, Toufailia et al. (2016) studied hygienic behavior in Brazilian M. scutellaris, Scp. depilis, and Ttr. angustula. The authors also reported high levels of hygienic behavior after 48 h in all three species (>60%). A significant negative correlation between freeze-killed brood removal and the frequency of deformed Scp. depilis was found, implying a link between hygienic behavior and disease presence in stingless bee colonies.

Interestingly, although hygienic behavior is present in honey bees and stingless bees, marked diffences exist between both taxa. The levels of pupa removal of stingless bees is generally above 60% (in some species >90%) while in the honey bee it is usually <50% (Medina-Medina et al. 2009; Nunes-Silva et al. 2009; Toufailia et al. 2016). Moreover, hygienic behavior has been recorded in all colonies of stingless bees studied, while in honey bees, the frequency of colonies exhibiting hygienic behavior is low (Bigio et al. 2013).

In addition, stingless bees remove infected cells completely, not just cappings, as occurs in the honey bee (Medina-Medina et al. 2009). The elimination of cocoons and waste in brood cells, reduces potential sources of infection to adults, brood, and food stores (Medina-Medina et al. 2014). In contrast, in the honey bee, workers can eliminate infected individuals, but potentially infected waste is left in the colony. In Meliponini, a combination of a high level of hygienic behavior (high rate of brood removal) and complete elimination of potential sources of infection seem highly effective mechanisms to face and cope with disease. Low rates of infection and spread of disease may result from the stingless bee system of pathogen management (Toufailia et al. 2016; Díaz et al. 2017).

5.5 Communication by Chemical Means

In the highly eusocial insects information is extensively passed on among individuals using chemical signals (Wilson 1990). In the stingless bees, the identification of specific chemical signals as well as evidence on their involvement in communication are still comparatively limited. Nonetheless, the amount of information on the chemical world of stingless bees has significantly increased in the last two decades. Thanks to new methods of analysis and the possibility of artificially producing many of the identified compounds greatly improve the possibility of new and exciting discoveries on the chemical ecology of these insects (Couvillon and Ratnieks 2008; Jarau 2009; Nunes et al. 2009a).

A distinctive feature of stingless bees is the impressive number and diversity of chemical compounds on individuals and nests (Leonhardt et al. 2015). Some of them, probably the majority, only serve a structural purpose. Nonetheless, those conveying information or semiochemicals can have important intra- or interspecific effects (Wyatt 2003). Those semiochemicals mediating intraspecific communication are known as pheromones (Free 1987). Pheromones are compounds produced in glands and secreted externally, serving as signals that affect the behavior, development, and/or physiology of conspecifics (Free 1987). Those semiochemicals acting at interspecific level are known as allelochemicals or allomones (Free 1987; Jarau 2009).

Apart from their type of action, semiochemicals can work as signals or cues (Barth et al. 2008; Jarau 2009). A semiochemical is considered a signal if it evolved to convey specific information. In contrast, a cue is incidentally used to transmit information, but did not evolve specifically for that purpose (Barth et al. 2008).

One aspect of the life of stingless bee colonies, in which chemicals are frequently involved, is the collection of food. From the food source itself, to the transmission of information on location and direction, chemical signals are involved in the process. Floral fragrances are important sources of chemicals that attract potential visitors. Fragrances serve the plant guiding pollinators looking for potential food (Raguso 2001). Indeed, flowers have evolved fragrance to attract pollinators evoking discriminatory behavior (Proctor et al. 1996; Chittka and Thomson 2001). Bees use fragrances to find flowers (and rewards), and they are capable of associating them with specific food sources (Chittka and Thomson 2001; Raguso 2001). The smell of food is of particular relevance to species with relative simple mechanisms of communication, like Plebeia . In these species, foragers carry the smell of flowers which seems the almost exclusive mechanism used by nestmates to find such sources (Jarau 2009). The smell of food can be important in species with more sophisticated mechanisms of food exploitation too.

A higher level of chemical communication involves the use of scent marks left by the workers when visiting food sources. Species of Tetragonisca, Scaptotrigona, Nannotrigona, and some Melipona use marks to find (or reject) flowers that have been previously visited by nestmates. Experiments using artificial feeders show that sources previously visited can be more attractive compared to non- visited ones (Villa and Weiss 1990). Interestingly, scent marks may equally attract nestmates and non-nest mates indicating that such cues are not colony specific (Nieh 2004; Nieh et al. 2004; Jarau 2009).

The use of Scent marks may depend on reward accessibility. In Tr. fulviventris, if nectar is easily obtained, with little energy invested in the process, scent marks are less intensely used. However, if food is difficult to obtain, bees more frequently leave scent marks on them. Curiously, scent marks seem to have a repellent effect in some situations, and flowers previously visited can become less attractive (Goulson et al. 2001). Evidently, scent marks can have different effects depending on the context in which food is presented. Scent marks are also involved in interspecific interactions; artificial feeders first visited by M. beecheii resulted less attractive to Tr. corvina foragers (Boogert et al. 2006).

Although the effects of scent marks had been known, their origin had been debatable. Initial works in Melipona suggested the anal glands as the source of scent marks (Kerr and Rocha 1988; Aguilar and Sommeijer 2001). However, there was no clear correlation between gland depositions and attraction to food sources (Aguilar and Sommeijer 2001). Moreover, feeders intensively marked were not visited at a similar rate (Nieh 1998; Hrncir et al. 2004a), suggesting that anal glands were not the origin of scent marks in Melipona.

Another candidate source of scent marks are the tendon glands inside the femur and tibia. These glands open at the base of the pretarsus on the distal portion of the legs. When the external duct of the tendon gland was obstructed in M. seminigra workers visiting a feeder, significantly less visits occurred, compared to feeders visted by workers with intact glands (Hrncir et al. 2004a). In addition, when extracts of the tendon glands were experimentally applied to feeders, the number of visits increased. Such results suggest tendon glands as a more plausible origin of scent marks. Chemical analysis of tendon gland extracts revealed that frequent compounds are saturated hydrocarbons (≥10%, pentacosane and heptacosane), and their corresponding alkenes (Jarau et al. 2004).

Although scent marks are important in food location, the effect can be considered a cue rather than a signal. The scent is left as the bee walks on the food, and is therefore left passively. Foragers do not seem to leave scent marks on food sources on purpose.

Another group of chemicals used in food location can be effectively considered signals. They evolved specifically to guide nestmates to food sources (Schorkopf et al. 2007; Barth et al. 2008). These signals are collectively known as trail pheromones and have been documented in various genera of stingless bees (Trigona, Scaptotrigona, Geotrigona, Cephalotrigona, and Oxytrigona). Trail pheromones represent a more efficient method for locating food sources compared to scent marks. They can guide nestmates across distance but also altitude. The indication of altitude is an important feature of food location in stingless bees in rain forests, which is absent in A. mellifera (Jarau 2009). With the help of the glossa, successful foragers leave pheromone droplets at regular intervals building a path from the food source to the nest, that can be followed by nestmates. Droplets are usually deposited more frequently in proximity to the food source (Schorkopf et al. 2007). It has been shown that trail pheromones are produced in the labial glands of the head, and not the mandibular glands, as was originally believed (Schorkopf et al. 2007, 2009).

Most species of stingless bee use either scent marks or trail pheromones as guides to food sources. Nonetheless, there also seem to be some forms of food communication not mediated by such chemical methods. A study in Pt. orizabaensis showed that workers of this species can rapidly recruit nestmates to food sources, but no evidence was found for the use of marks from the legs nor trail pheromones produced in the labial glands (Flaig et al. 2016). Chemical signals (marks or trails) are useful to colony members for food location. However, there is also the potential risk of such signals being used by conspecific and heterospecific competitors, a form of “espionage ” defined as eavesdropping (Nieh et al. 2004). The risk of eavesdropping may represent a strong selective force upon mechanisms of food collection based on chemical cues. Perhaps, “hidden” food communication in some species (as Pt. orizabaensis; Flaig et al. 2016) may be the evolutionary response to avoid the risk of eavesdropping by competitors (Lichtenberg et al. 2011). There may be still some interesting forms of food communication in stingless bees waiting to be discovered.

The mandibular glands of stingless bees may not be involved in recruitment to food sources, but they participate in other forms of chemical communication. Many compounds found in the mandibular glands are highly volatile, disseminating rapidly. When threatened, workers of many species spread their mandibles, possibly releasing alarm pheromones. One alarm pheromone frequently found in the mandibular glands of stingless bees is 2-heptanol (Keeping et al. 1982; Smith and Roubik 1983; Johnson et al. 1985; Engels et al. 1987; Cruz-Lopez et al. 2007). This compound is also found in honey bee workers (Free 1987). Nonetheless, in some species, like M. beecheii, 2-heptanol has not been detected in the mandibular glands of workers (Cruz-Lopez et al. 2005). Interestingly, the mandibular secretions of males may trigger an aggressive response of Scaptotrigona and Partamona workers. Males of these species seem to represent a first front in colony defense producing alarm signals that alert workers (Schorkopf 2016). An extreme case of the use of the mandibular glands in defense, is in species of the genus Oxytrigona . The mandibular glands of Oxytrigona workers produce caustic chemicals (mainly formic acid) that burn the skin when biting (Roubik et al. 1987).

Compounds produced in the mandibular glands of stingless bee gynes and males seem to play an important role during sexual attraction (Engels et al. 1990). However, no particular sexual attractant has yet been identified in mandibular bouquets of stingless bees.

Another important aspect of chemical communication in stingless bees is nestmate recognition . Stingless bees, like other highly eusocial insects need rapid and efficient identification of nestmates from potential intruders (Nunes et al. 2008). Most evidences from highly eusocial insects, including bees, suggest that the information for nestmate recognition is encoded in the hydrocarbons covering the cuticle (Vander Meer and Morel 1998; Lenoir et al. 2001; van Zweden and D’Ettorre 2010).

Cuticular hydrocarbons are hydrophobic compounds protecting the insect from water loss (Gibbs 1995). There are differences in the volatility of cuticular compounds which depend on the length of the molecule, the presence of unsaturated bonds and methylation. Unsaturated hydrocarbons can be highly volatile, and are good candidates for recognition cues (Gibbs and Pomonis 1995). Indeed, in the stingless bees alkenes and alkadienes seem mainly responsible for nestmate recognition (Jungnickel et al. 2004; Buchwald and Breed 2005; Pianaro et al. 2007; Nunes et al. 2008; Nascimento and Nascimento 2012; Septanil et al. 2012). One indication of the importance of unsaturated hydrorcarbons in stingless bee recognition is a highly diversified production of alkene isomers in this taxon (Martin et al. 2017). Cuticular hydrocarbons seem predominantly of genetic origin, but can also be acquired from the environment (Breed et al. 1985; Page Jr et al. 1991; Leonhardt et al. 2015; Gutiérrez et al. 2016). In the case of stingless bees, cerumen has been proposed as a candidate for external recognition hydrocarbons (Nunes et al. 2011), although this hypothesis has not been confirmed (Jones et al. 2012). Similarly, resin-derived terpenoids substantially enrich the cuticular profile of stingless bees, but their role in nestmate recognition is still unclear (Leonhardt et al. 2010a, b; Leonhardt et al. 2015).

It seems that the mixture of cuticular hydrocarbons provides an individual fingerprint. Guard bees are in charge of discriminating nestmates from potential intruders. However, individual fingerprints change continuously, and guards must constantly update their internal recognition pattern (Couvillon and Ratnieks 2008; Nunes et al. 2008; Nascimento and Nascimento 2012). Interestingly, although individual fingerprints show variation, nestmate fingerprints are more similar to the guards’ than non-nestmates (Couvillon and Ratnieks 2008; Nascimento and Nascimento 2012). Guard bees compare the chemical fingerprint of individuals entering the nest with a pattern in their brain of guards, if these do not match aggression is elicited against non-nestmates (Nash and Boomsma 2008; van Zweden and D’Ettorre 2010; Nunes et al. 2011). It is suggested that in stingless bees a system based on undesirably absent compounds is used for the recognition of intruders (Couvillon and Ratnieks 2008).

Nestmate recognition is important for the protection of food and materials in the nest. However, specialized intruders have evolved chemical disguise or insignificance to avoid recognition (Lenoir et al. 2001; Martin et al. 2007; 2010; van Zweden and D’Etorre 2010). Lestrimelitta workers are specialized cleptobionts which during nest raids release large amounts of citral (lemon-smelling pheromone) produced in the mandibular glands (Sakagami et al. 1993). Citral may weaken the defensive response of hosts by disrupting chemical recognition (Blum et al. 1970). However, no conclusive evidence for citral as a masking allomone has been found, and its use by Lestrimelitta seems to vary depending on host species, and the context in which the attacks are conducted (Sakagami et al. 1993). In some hosts, citral releases aggression, but in others like Fr. varia, compounds from the labial glands of Lestrimelitta could possibly have a repellent effect (von Zuben et al. 2016; Table 5.2)
Table 5.2

Some candidate semiochemicals detected on stingless bees with their origin and function

Interestingly, Lestrimelitta is host selective (Sakagami et al. 1993; Quezada-Euán and González-Acereto 2002). It is not clear how these obligate cleptobionts select their hosts. It has been suggested that the quality of reserves and aggressive response of the host, and perhaps genetic factors, may be involved in host selection. It is also possible that specialization may be part of this system, and scouts gaining easier access to some species could learn by association (Sakagami et al. 1993; Jarau 2009).

Lestrimelitta mass attacks would require some sort of nestmates recruitment (Fig. 5.9). It is possible that Lestrimelitta scouts previously enter nests to obtain some sort of information to select their prey (Sakagami et al. 1993).

Similar to other social cleptobionts Lestrimelitta scouts may use chemical deception or insignificance to avoid recognition (Quezada-Euán et al. 2013). To evaluate this possibility, the similarity of cuticular profiles was compared between five potential host species and L. niitkib from the Yucatan Peninsula. The study involved assessing the speed to recognize L. niitkib workers by guards of species that are frequently raided, and others that are not raided. Interestingly, L. niitkib cuticular profile was not insignificant, but remarkably similar to some of its preferred hosts. Alkenes C27:1 and C29:1 were predominant in two frequently raided species (N. perilampoides and Pb. frontalis) and L. niitkib. The workers of chemically similar species also took longer to react to L. niitkib compared with dissimilar ones, suggesting that cleptobionts may pass unnoticed by guards. It was noted that cuticular similarities may arise as a result of the phylogenetic closeness of Lestrimelitta with Nannotrigona and Plebeia (Rasmussen and Cameron 2010). The results of this study indicate that chemical deception may be used in combination with other forms of host attack by these obligate cleptobionts (Quezada-Euán et al. 2013).

Apart as clues in nestmate recognition, cuticular hydrocarbons possibly indicate the status of colony members (Cruz-Landim et al. 2012). Differences between the cuticular profile of gynes and physogastric queens have been reported in various species (Nunes et al. 2009a, b). Curiously, the cuticular profiles of workers seem to be more similar to those of males than queens (Borges et al. 2012). Although cuticular compounds generally indicate the presence of the queen to members of her colony (Engels 1987), a notable finding, is that the cuticular hydrocarbons of the queen in Frs. schrotkyii seem also responsible of the ovarian suppression of workers, a process somehow similar to that in A. mellifera (Nunes et al. 2014a).

In spite of the well-known role of chemical cues and pheromones in the attraction of mates in other insects, evidence is still scarce in stingless bees (Billen and Morgan 1998; Grüter and Keller 2016). In Scp. postica, secondary alcohols (Engels et al. 1987) and hydrocarbons of the queen cuticle (Flach et al. 2006), seem to be involved in the attraction of mates. Flach et al. (2006) found that some chemicals in the fragrance of an orchid flower are remarkably similar to the cuticular profile of Scp. postica queens, and deceive males of this species to pollinate the plant. In Scp. mexicana, males were capable of identifying virgin and physogastric queens by their chemical profiles. The relative amounts of 2-nonanol and other alcohols of the queen’s cuticle seem to act as discriminating cues (Verdugo-Dardón et al. 2011). Similarly, isopropyl-hexanoate, a compound found on the abdomens of gynes of Ttr. angustula, elicited a strong electroantennogram response in the males of this species, suggesting its possible role as a sexual attractant (Fierro et al. 2011).

A summary of candidate semiochemicals and their suggested contribution in different aspects of the communication in stingless bees is presented in Table 5.2.

5.6 Communication by Physical Means

The best studied context in which bees frequently use physical cues is in the communication during food exploitation. In the honey bee, the use of dances to indicate distance and direction to the food as well as in recruitment is well known (Seeley 1985, 1995). The stingless bees also use physical mechanisms to communicate (vibrations, runs, sounds), but the information conveyed in many of these signals is not well understood (Nieh et al. 2003; Hrncir et al. 2004b; Schmidt et al. 2008).

When foragers return to their nests after finding a source of food, they become agitated, run rapidly around the nest, and frequently bump into other workers (Hrncir et al. 2004a). These collisions or bumps are collectively known as jostling, and have been interpreted as a way through which foragers communicate their success in finding food, or may be used to recruit other foragers (Hrncir et al. 2004a; Barth et al. 2008). In M. quadrifasciata, the number of workers engaging in syrup collection increases in relation with the number of individuals being jostled by scouts (Hrncir et al. 2000).

In addition to jostling, successful foragers can also use the thoracic muscles to vibrate the substrate, producing sounds and air currents. Workers probably use the subgenual organ of their legs or the Johnston’s organ of the antennae to perceive such vibrations (Hrncir et al. 2006; Barth et al. 2008). It has been detected that vibrations encoding information related with food finding are usually in the range of 300–600 Hz, and that foragers frequently perform these vibrations when transferring food to nest bees (Hrncir et al. 2006). In M. seminigra, foragers returning from the field frequently shake some apparently inactive workers in the nests, but it is not clear if this stimulates them to start foraging (Hrncir et al. 2004b).

Mechanical cues seem to indicate a food resource, but whether they encrypt some other information related to distance and orientation (as occurs in A. mellifera), has not been conclusively demonstrated in stingless bees. In some Melipona, no correlation has been found between the number and intensity of the vibrations performed by successful foragers with the distance or orientation to the food source (Hrncir et al. 2000; Hrncir et al. 2004b). In contrast, studies in other species have detected significant correlation between the intensity and frequency of the vibrations performed by foragers with the distance to food (Nieh 1998; Nieh and Roubik 1998). In M. seminigra, there is a great deal of variation in the pulsations of different foragers coming from the same food source, raising doubts about their validity as reliable indicators of distance (Hrncir et al. 2004b). It has been suggested that the contrasting results found in Melipona may relate to differences in the ability to communicate spatial dimensions among species (Nieh 2004).

A clear evidence for the transmission of information by means of vibrations is related to the quality of food. In various species, it has been consistently found that the duration and frequency of thorax vibrations increase when the sugar content of the food increases (M. costaricensis: Aguilar and Briceño 2002; M. mandacaia, M. bicolor: Nieh et al. 2003; M. seminigra: Hrncir et al. 2004b; N. testaceicornis: Schmidt et al. 2008).

Bees live most of their lives in obscurity. However, they use vision in external activities. Workers use ultraviolet light to find nectar guides on flowers and can detect polarized light (Winston 1987; Chittka and Thomson 2001). It is documented that stingless bees are capable of associating color with different food sources (Villa and Weiss 1990). Workers of M. seminigra can use optic flow (moving images) in route to the food source to obtain an indication of distance. However, whether this information is transmitted to other workers and how it is done remain unclear (Hrncir et al. 2003).

The spectra of light may be differently perceived by stingless bee species. In a comparative study, M. mondury preferred UV-reflecting over UV-absorbing bee-blue-green objects, whereas M. quadrifasciata showed an opposite preference. This result suggests that differential visual adaptations may have evolved to avoid interspecific competition during food collection in stingless bees (Koethe et al. 2016).

Stingless bees learn rapidly and are capable of associating time and space with food availability (Breed et al. 2002). Workers can learn the location and the time when food is available and can remember these traits for over long periods of time. Learning and association have only been found in eusocial Hymenoptera (Breed et al. 2002). When foraging, some visual cues, mainly the presence of other bees on the food, could be used as additional guides or repellents to such sources (Sommerlandt et al. 2014).

Evidently, stingless bees are capable of communicating food location and other important features of their environment to other colony members. However, the cues or signals they use, how they are transmitted, and the information they may convey, are still not completely revealed.


  1. Aguilar I, Briceño D (2002) Sounds in Melipona costaricensis (Apidae: Meliponini): effect of the sugar concentration and nectar source distance. Apidologie 33:375–388CrossRefGoogle Scholar
  2. Aguilar I, Sommeijer M (2001) The deposition of anal excretions by Melipona favosa foragers (Apidae: Meliponinae): behavioural observations concerning the location of food sources. Apidologie 32:37–48CrossRefGoogle Scholar
  3. Aparecido-Pereira R, Morais MM, Gioli LD, Santos NF, Rossi MA, Bego LR (2006) Comparative morphology of reproductive and trophic eggs in Melipona bees (Apidae, Meliponini). Braz J Morphol Sci 23:349–354Google Scholar
  4. Avila B, Moo-Valle H, Valladares P, Camposeco F, Quezada-Euán JJG (2005) Descripción del proceso de aprovisionamiento y oviposición en colonias de Melipona beecheii (Apidae: Meliponini). Reporte de investigación, opción apicultura. FMVZ-Universidad Autónoma de Yucatán, Maestría en Producción Animal TropicalGoogle Scholar
  5. Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol A 194:313–327CrossRefGoogle Scholar
  6. Bian Z, Fales HM, Blum MS, Jones TH, Rinderer TE, Howard DF (1984) Chemistry of cephalic secretion of fire bee Trigona (Oxytrigona) tataira. J Chem Ecol 10:451–461PubMedCrossRefPubMedCentralGoogle Scholar
  7. Biesmeijer JC (1997) The organisation of foraging in stingless bees of the genus Melipona; an individual approach. Ph.D. thesis, Utrecht University, Utrecht, 263 ppGoogle Scholar
  8. Biesmeijer JC, Toth E (1998) Individual foraging, activity level and longevity in the stingless bee Melipona beecheii in Costa Rica (Hymenoptera, Apidae, Meliponinae). Insect Soc 45:427–443CrossRefGoogle Scholar
  9. Bigio G, Schürch R, Ratnieks FLW (2013) Hygienic behaviour in honey bees (Hymenoptera: Apidae): effects of brood, food, and time of the year. J Econ Entomol 106:2280–2285PubMedCrossRefPubMedCentralGoogle Scholar
  10. Billen J, Morgan ED (1998) Pheromone communication in social insects: sources and secretions. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 3–33Google Scholar
  11. Blum MS, Crewe RM, Kerr WE, Keith LH, Garrison AW, Walker MM (1970) Citral in stingless bees: isolation and functions in trail laying and robbing. J Insect Physiol 16:1637–1648PubMedCrossRefPubMedCentralGoogle Scholar
  12. Borges AA, Ferreira-Caliman MJ, Nascimento FS, Campos LAO, Tavares MG (2012) Characterization of cuticular hydrocarbons of diploid and haploid males, workers and queens of the stingless bee Melipona quadrifasciata. Insect Soc 59:479–486CrossRefGoogle Scholar
  13. Boogert NJ, Hofstede FE, Aguilar Monge I (2006) The use of food source scent marks by the stingless bee Trigona corvina (Hymenoptera: Apidae): the importance of the depositor’s identity. Apidologie 37:366–375CrossRefGoogle Scholar
  14. Breed MD, Butler L, Stiller TM (1985) Kin discrimination by worker honey bees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061PubMedCrossRefPubMedCentralGoogle Scholar
  15. Breed MD, Stocker EM, Baumgartner LK, Vargas E (2002) Time-place learning and the ecology of recruitment in a stingless bee, Tr. amalthea (Hymenoptera, Apidae). Apidologie 33:251–258CrossRefGoogle Scholar
  16. Breed MD, Cook C, Krasnec MO (2012) Cleptobiosis in social insects. Psyche. Article ID 484765Google Scholar
  17. Buchwald R, Breed MD (2005) Nestmate recognition cues in the stingless bee Trigona fulviventris. Anim Behav 70:1331–1337CrossRefGoogle Scholar
  18. Camargo JMF, Garcia MVB, Junior ERQ, Castrillon A (1992) Notas previas sobre a bionomia de Ptilotrigona lurida (Hymenoptera, Apidae, Meliponinae): associação de leveduras em pólen estocado. Boletim do Museu Paraense Emílio Goeldi 8:391–395Google Scholar
  19. Camargo JMF, Pedro SRM (2007) Meliponini Lepeletier, 1836. In: Moure JS (ed) Catalogue of the bees (Hymenoptera, Apoidea) in the Neotropical region. Sociedade Brasileira de Entomologia, Curitiba, pp 272–578Google Scholar
  20. Cardoso-Júnior CAM, Pereira Silva R, Araújo Borges N, de Carvalho WJ, Walter SL, Paulino Simões ZL, Bitondi MMG, Ueira Vieira C, Bonetti AM, Hartfelder K (2017a) Methyl farnesoate epoxidase (mfe) gene expression and juvenile hormone titers in the life cycle of a highly eusocial stingless bee, Melipona scutellaris. J Insect Physiol 101:185–194PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cardoso-Júnior CAM, Fujimura PT, Santos-Júnior CD, Borges NA, Ueira-Vieira C, Hartfelder K, Goulart LR, Bonetti AM (2017b) Epigenetic modifications and their relation to caste and sex determination and adult division of labor in the stingless bee Melipona scutellaris. Genet Mol Biol 40(1):61–68PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chittka L, Thomson JD (2001) Cognitive ecology of pollination, animal behavior and floral evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Choo YM, Lee KS, Yoon HJ, Kim BY, Sohn MR et al (2010) Dual strategy of bee venom serine protease: prophenoloxidase-activating factor in arthropods and fibrin(ogen)olytic enzyme in mammals. PLoS One 5:e10393PubMedPubMedCentralCrossRefGoogle Scholar
  24. Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an ‘undesirable-absent’ recognition system. Behav Ecol Sociobiol 62:1099–1105CrossRefGoogle Scholar
  25. Crespi BJ (1992) Cannibalism and trophic eggs in subsocial and eusocial insects. In: Elgar MA, Crespi BJ (eds) Cannibalism, ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 176–213Google Scholar
  26. Cruz-Landim C (2000) Ovarian development in Meliponine bees (Hymenoptera: Apidae): the effect of queen presence and food on worker ovary development and egg production. Genet Mol Biol 23:83–88CrossRefGoogle Scholar
  27. Cruz-Landim C, Ferreira-Caliman MJ, Gracioli-Vitti LF, Zucchi R (2012) Correlation between mandibular gland secretion and cuticular hydrocarbons in the stingless bee Melipona quadrifasciata. Genet Mol Res 11:966–977PubMedCrossRefPubMedCentralGoogle Scholar
  28. Cruz-Lopez L, Malo EA, Morgan ED, Rincon M, Guzman M, Rojas JC (2005) Mandibular gland secretion of Melipona beecheii: chemistry and behavior. J Chem Ecol 31:1621–1632PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cruz-Lopez L, Aguilar S, Malo EA, Rincon M, Guzman M, Rojas JC (2007) Electroantennogram and behavioral responses of workers of the stingless bee Oxytrigona mediorufa to mandibular gland volatiles. Entomol Exp Appl 123:43–47CrossRefGoogle Scholar
  30. Dade HA (1985) Anatomy and dissection of the honeybee. International Bee Research Association, LondonGoogle Scholar
  31. Daneels EL, Van Vaerenberg M, Debyser G, Devreese B, Graaf DC d (2015) Honeybee venom proteome profile of queens and winter bees as determined by a mass spectrometric approach. Toxins 7:4468–4483CrossRefGoogle Scholar
  32. Díaz S, de Souza Urbano S, Caesar L, Blochtein B, Sattler A, Zuge V, Haag KL (2017) Report on the microbiota of Melipona quadrifasciata affected by a recurrent disease. J Invertebr Pathol 143:35–39PubMedCrossRefGoogle Scholar
  33. dos Santos CG, Blochtein B, Megiolaro FL, Imperatriz-Fonseca VL (2010) Age Polyethism in Plebeia emerina (Friese) (Hymenoptera: Apidae) colonies related to propolis handling. Neotrop Entomol 39:691–696PubMedCrossRefPubMedCentralGoogle Scholar
  34. dos Santos CF, Ferreira-Caliman MJ, Nascimento FS (2015) An alien in the group: eusocial male bees sharing nonspecific reproductive aggregations. J Insect Sci 15:157PubMedPubMedCentralCrossRefGoogle Scholar
  35. Drumond PM, Zucchi R, Oldroyd BP (2000) Description of the cell provisioning and oviposition process of seven species of Plebeia Schwarz (Apidae, Meliponini), with notes on their phylogeny and taxonomy. Insect Soc 47:99–112CrossRefGoogle Scholar
  36. Eardley CD (2004) Taxonomic revision of the African stingless bees (Apoidea: Apidae: Apinae: Meliponini). Afr Plant Protect 10:63–96Google Scholar
  37. Engels W (1987) Pheromones and reproduction in Brazilian stingless bees. Memorias Instituto Oswaldo Cruz, Rio de Janeiro 82(Suppl III):35–45CrossRefGoogle Scholar
  38. Engels E, Engels W, Schroder W, Francke W (1987) Intranidal worker reactions to volatile compounds identified from cephalic secretions in the stingless bee, Scaptotrigona postica (Hymenoptera, Meliponinae). J Chem Ecol 13:371–386PubMedCrossRefPubMedCentralGoogle Scholar
  39. Engels W, Engels E, Lübke G, Schröder W, Francke W (1990) Volatile cephalic secretions of drones, queens and workers in relation to reproduction in the stingless bee, Scaptotrigona postica. Entomologia Generalis 15:91–101CrossRefGoogle Scholar
  40. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M et al (2006) Immune pathways and defence mechanisms in honeybees Apis mellifera. Insect Mol Biol 15:645–656PubMedPubMedCentralCrossRefGoogle Scholar
  41. Fierro MM, Cruz-López L, Sánchez D, Villanueva-Gutiérrez R, Vandame R (2011) Queen volatiles as a modulator of Tetragonisca angustula drone behavior. J Chem Ecol 37:1255–1262PubMedCrossRefPubMedCentralGoogle Scholar
  42. Flach A, Marsaioli AJ, Singer RB, Amaral M d CE, Menezes C, Kerr WE, Batista-Pereira LG, Correa AG (2006) Pollination by sexual mimicry in Mormolyca ringens: a floral chemistry that remarkably matches the pheromones of virgin queens of Scaptotrigona sp. J Chem Ecol 32:59–70PubMedCrossRefPubMedCentralGoogle Scholar
  43. Flaig IC, Aguilar I, Schmitt T, Jarau S (2016) An unusual recruitment strategy in a mass-recruiting stingless bee, Partamona orizabaensis. J Comp Physiol A 202:679–690CrossRefGoogle Scholar
  44. Francke W, Schroder W, Engels E, Engels W (1983) Variation in cephalic volatile substances in relation to worker age and behavior in the stingless bee, Scaptotrigona postica. Z Naturforsch 38c:1066–1068CrossRefGoogle Scholar
  45. Free JB (1987) Pheromones of social bees. Cornell University Press, IthacaGoogle Scholar
  46. Gibbs A (1995) Physical properties of insect curticular hydrocarbons: model mixtures and lipid interactions. Comp Biochem Physiol 112B:667–672CrossRefGoogle Scholar
  47. Gibbs A, Pomonis JG (1995) Physical properties of insect cuticular hydrocarbons: the effects of chain length, methyl-branching and unsaturation. Comp Biochem Physiol 112B:243–249CrossRefGoogle Scholar
  48. Gloag R, Heard T, Beekman M, Oldroyd B (2008) Nest defence in a stingless bee: what causes fighting swarms in Trigona carbonaria (Hymenoptera, Meliponini)? Insect Soc 55:387–391CrossRefGoogle Scholar
  49. Gordon DM (2016) From division of labor to the collective behavior of social insects. Behav Ecol Sociobiol 70:1101–1108PubMedCrossRefGoogle Scholar
  50. Goulson D, Chapman JW, Hughes WOH (2001) Discrimination of unrewarding flowers by bees; direct detection of rewards and use of repellent scent marks. J Insect Behav 14:669–678CrossRefGoogle Scholar
  51. Greco MK, Hoffmann D, Dollin A, Duncan M, Spooner-Hart R, Neumann P (2010) The alternative pharaoh approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97:319–323PubMedCrossRefGoogle Scholar
  52. Grüter C, Menezes C, Imperatriz-Fonseca VL, Ratnieks FLW (2012) A morphologically specialized soldier caste improves colony defence in a Neotropical eusocial bee. Proc Natl Acad Sci USA 109:1182–1186PubMedCrossRefPubMedCentralGoogle Scholar
  53. Grüter C, Keller L (2016) Inter-caste communication in social insects. Curr Opin Neurobiol 38:6–11PubMedCrossRefPubMedCentralGoogle Scholar
  54. Grüter C, von Zuben LG, Segers FHID, Cunningham JP (2016) Warfare in stingless bees. Insect Soc 63:223–236CrossRefGoogle Scholar
  55. Grüter C, Segers FHID, Menezes C, Vollet-Neto A, Falcón T, von Zuben L, Bitondi MMG, Nascimento FS, Almeida EAB (2017) Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees. Nat Commun 8:4PubMedPubMedCentralCrossRefGoogle Scholar
  56. Gutiérrez E, Ruiz D, Solís T, May-Itzá W d J, Moo-Valle H, Quezada Euán JJG (2016) Does larval food affect cuticular profiles and recognition in eusocial bees? A test on Scaptotrigona gynes (Hymenoptera: Meliponini). Behav Ecol Sociobiol 70:781–789CrossRefGoogle Scholar
  57. Hart AG, Ratnieks FLW (2001) Why do honey-bee (Apis mellifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system. Behav Ecol Sociobiol 49:244–250CrossRefGoogle Scholar
  58. Hart AG, Ratnieks FLW (2002) Task partitioned nectar transfer in stingless bees (Meliponini): work organisation in a phylogenetic context. Ecol Entomol 27:163–168CrossRefGoogle Scholar
  59. Hartfelder K, Bitondi MMG, Santana WC, Simões ZLP (2002) Ecdysteroid titers and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? J Insect Physiol 32:211–216Google Scholar
  60. Hartfelder K, Makert GR, Judice CC, Pereira GAG, Santana WC, Dallacqua R, Bitondi MMG (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37:144–163CrossRefGoogle Scholar
  61. Hermann HR (1984) Defensive mechanisms: general considerations. In: Hermann HR (ed) Defensive mechanisms in social insects. Praeger, New York, pp 1–31Google Scholar
  62. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  63. Hrncir M, Jarau S, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bees, Melipona scutellaris and M. quadrifasciata. II. Possible mechanisms of communication. Apidologie 31:93–113CrossRefGoogle Scholar
  64. Hrncir M, Jarau S, Zucchi R, Barth FG (2003) A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances. J Comp Physiol 189:761–768CrossRefGoogle Scholar
  65. Hrncir M, Jarau S, Zucchi R, Barth FG (2004a) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35:3–13CrossRefGoogle Scholar
  66. Hrncir M, Jarau S, Zucchi R, Barth FG (2004b) Thorax vibrations of a stingless bee (Melipona seminigra). II. Dependence on sugar concentration. J Comp Physiol A 190:549–560Google Scholar
  67. Hrncir M, Schmidt VM, Schorkopf DLP, Jarau S, Zucchi R, Barth FG (2006) Vibrating the food receivers: a direct way of signal transmission in stingless bees (Melipona seminigra). J Comp Physiol A 192:879–887CrossRefGoogle Scholar
  68. Jarau S (2009) Chemical communication during food exploitation in stingless bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects: ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 223–250CrossRefGoogle Scholar
  69. Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804PubMedCrossRefPubMedCentralGoogle Scholar
  70. Jarau S, Schulz CM, Hrncir M, Francke W, Zucchi R, Barth FG, Ayasse M (2006) Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, Trigona recursa. J Chem Ecol 32:1555–1564PubMedCrossRefPubMedCentralGoogle Scholar
  71. Johnson LK, Haynes LW, Carlson MA, Fortnum HA, Gorgas DL (1985) Alarm substances of the stingless bee, Trigona silvestriana. J Chem Ecol 11:409–416PubMedCrossRefPubMedCentralGoogle Scholar
  72. Jones SM, van Zweden JS, Grüter C, Menezes C, Alves DA, Nunes-Silva P, Czaczkes T, Imperatriz-Fonseca VL, Ratnieks FLW (2012) The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula. Behav Ecol Sociobiol 66:1–12CrossRefGoogle Scholar
  73. Jungnickel H, Velthuis HHW, Imperatriz-Fonseca VL, Morgan ED (2001) Chemical properties allow stingless bees to place their eggs upright on liquid larval food. Physiol Entomol 26:300–305CrossRefGoogle Scholar
  74. Jungnickel H, da Costa AJS, Tentschert J, Flávia E, Patricio LRA, Imperatriz-Fonseca VL, Drijfhout F, Morgan ED (2004) Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera: Apidae). J Insect Physiol 50:761–766PubMedCrossRefPubMedCentralGoogle Scholar
  75. Keeping MG, Crewe RM, Field BI (1982) Mandibular secretions of the old world stingless bee, Trigona gribodoi Magrettii: isolation, identification, and compositional changes with age. J Apic Res 21:65–73CrossRefGoogle Scholar
  76. Kerr WE, Lello E (1962) Sting glands in stingless bees—a vestigial character. J NY Entomol Soc 70:190–214Google Scholar
  77. Kerr WE, Rocha R (1988) Communicação em Melipona rufiventris e Melipona compressipes. Ciência e Cultura 40:1200–1202Google Scholar
  78. Kirchner WH, Lindauer M (1994) The causes of the tremble dance. Behav Ecol Sociobiol 35:303–308CrossRefGoogle Scholar
  79. Koedam D, Velthausz PH, van de Krift T, Dohmen MR, Sommeijer MJ (1996) Morphology of reproductive and trophic eggs and their controlled release by workers in Trigona (Tetragonisca) angustula Illiger (Apidae, Meliponinae). Physiol Entomol 21:289–296CrossRefGoogle Scholar
  80. Koethe S, Bossems J, Dyer AG, Lunau K (2016) Colour is more than hue: preferences for compiled colour traits in the stingless bees Melipona mondury and M. quadrifasciata. J Comp Physiol A 202:615–627CrossRefGoogle Scholar
  81. Kolmes SA (1985) An information-theory analysis of task specialization among worker honey bees performing hive duties. Anim Behav 33:181–187CrossRefGoogle Scholar
  82. Kwong WK, Medina LA, Koch H, Sing KW, Yu Soh EJ, Ascher JS, Jaffé R, Moran NA (2017) Dynamic microbiome evolution in social bees. Sci Adv 3:e1600513PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lapidge K, Oldroyd B, Spivak M (2002) Seven suggestive quantitative trait loci influence hygienic behavior of honeybees. Naturwissenschaften 89:565–568PubMedPubMedCentralGoogle Scholar
  84. Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599PubMedCrossRefPubMedCentralGoogle Scholar
  85. Leonhardt SD, Blüthgen N (2009) A sticky affair: resin collection by Bornean stingless bees. Biotropica 41:730–736CrossRefGoogle Scholar
  86. Leonhardt SD, Kaltenpoth M (2014) Microbial communities of three sympatric Australian stingless bee species. PLoS One 9:e105718PubMedPubMedCentralCrossRefGoogle Scholar
  87. Leonhardt SD, Jung LM, Schmitt T, Blüthgen N (2010a) Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting. Behav Ecol Sociobiol 64:1415–1423CrossRefGoogle Scholar
  88. Leonhardt SD, Zeilhofer S, Schmitt T (2010b) Stingless bees use terpenes as olfactory cues to find resin sources. Chem Senses 35:603–611PubMedCrossRefPubMedCentralGoogle Scholar
  89. Leonhardt SD, Wallace HM, Blüthgen N, Wenzel F (2015) Potential role of environmentally derived cuticular compounds in stingless bees. Chemoecology 25:159–167CrossRefGoogle Scholar
  90. Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65:763–774PubMedCrossRefPubMedCentralGoogle Scholar
  91. Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41–65–71CrossRefGoogle Scholar
  92. López-Uribe MM, Sconiers WB, Frank SD, Dunn RR, Tarpy DR (2016) Reduced cellular immune response in social insect lineages. Biol Lett 12:20150984PubMedPubMedCentralCrossRefGoogle Scholar
  93. Machado JO (1971) Simbiose entre as abelhas sociais brasileiras (Meliponinae, Apidae) e uma espécie de bactéria. Ciência e Cultura 23:625–633Google Scholar
  94. Martin SJ, Jenner EA, Drijfhout FP (2007) Chemical deterrent enables a social parasitic ant to invade multiple hosts. Proc R Soc B 274:2717–2721PubMedCrossRefPubMedCentralGoogle Scholar
  95. Martin SJ, Carruthers JM, Williams PH, Drijfhout FP (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in bumblebees. J Chem Ecol 36:855–863PubMedCrossRefPubMedCentralGoogle Scholar
  96. Martin SJ, Shemilt S, da S Lima CB, de Carvalho CAL (2017) Are isomeric alkenes used in species recognition among neo-tropical stingless bees (Melipona spp). J Chem Ecol 43:1066–1072Google Scholar
  97. McFrederick SQ, Cannone JJ, Gutell RR, Kellner K, Plowes RM, Mueller UG (2013) Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl Environ Microbiol 79:1803–1812PubMedPubMedCentralCrossRefGoogle Scholar
  98. McFrederick SQ, Wcislo WT, Taylor DR, Ishak HD, Dowd SE et al (2012) Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol Notes 21:1754–1768CrossRefGoogle Scholar
  99. Medina-Medina LA, Hart AG, Ratnieks FLW (2009) Hygienic behavior in the stingless bees Melipona beecheii and Scaptotrigona pectoralis (Hymenoptera: Meliponini). Genet Mol Res 8:571–576CrossRefGoogle Scholar
  100. Medina-Medina LA, Hart AG, Ratnieks FLW (2014) Waste management in the stingless bee Melipona beecheii Bennett (Hymenoptera: Apidae). Sociobiology 61:428–434CrossRefGoogle Scholar
  101. Medina RG, Fairbairn DJ, Bustillos A, Moo-Valle H, Medina S, Quezada-Euán JJG (2016) Variable patterns of intraspecific sexual size dimorphism and allometry in three species of eusocial corbiculate bees. Insect Soc 63:493–500CrossRefGoogle Scholar
  102. Menezes C, Vollet-Neto A, León Contrera FA, Venturieri GC, Imperatriz-Fonseca VL (2013) The role of useful microorganisms to stingless bees and stingless beekeeping. In: Vit P, Pedro SRM, Roubik DW (eds) Pot honey: a legacy of stingless bees. Springer, New York, pp 153–172CrossRefGoogle Scholar
  103. Menezes C, Vollet-Neto A, Marsaioli AJ, Zampieri D, Fontoura IC, Luchessi AD, Imperatriz-Fonseca VL (2015) A Brazilian social bee must cultivate fungus to survive. Curr Biol 25:2851–2855PubMedCrossRefPubMedCentralGoogle Scholar
  104. Michener CD (1974) The social behavior of the bees: a comparative study. Belknap Press, Harvard University, CambridgeGoogle Scholar
  105. Morais PB, Calaça PSST, Rosa CA (2013) Microorganisms associated with stingless bees. In: Vit P, Pedro SRM, Roubik DW (eds) Pot honey: a legacy of stingless bees. Springer, New York, pp 173–186CrossRefGoogle Scholar
  106. Nascimento DL, Nascimento FS (2012) Acceptance threshold hypothesis is supported by chemical similarity of cuticular hydrocarbons in a stingless bee, Melipona asilvai. J Chem Ecol 38:1432–1440PubMedCrossRefPubMedCentralGoogle Scholar
  107. Nash DR, Boomsma JJ (2008) Communication between hosts and social parasites. In: D’Ettorre P, Hughes DP (eds) Sociobiology of communication: an interdisciplinary perspective. Oxford University Press, Oxford, pp 55–80CrossRefGoogle Scholar
  108. Nieh JC (1998) The role of a scent beacon in the communication of food location by the stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:47–58CrossRefGoogle Scholar
  109. Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182CrossRefGoogle Scholar
  110. Nieh JC, Roubik DW (1995) A stingless bee (Melipona panamica) indicates food location without using a scent trail. Behav Ecol Sociobiol 37:63–70CrossRefGoogle Scholar
  111. Nieh JC, Roubik DW (1998) Potential mechanisms for the communication of height and distance by a stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:387–399CrossRefGoogle Scholar
  112. Nieh JC, Tautz J, Spaethe J, Bartareau T (1999) The communication of food location by a primitive stingless bee, Trigona carbonaria. Zoology 102:238–246Google Scholar
  113. Nieh JC, Contrera FAL, Rangel J, Imperatriz-Fonseca VL (2003) Effect of food location and quality on recruitment sounds and success in two stingless bees, Melipona mandacaia and Melipona bicolor. Behav Ecol Sociobiol 55:87–94CrossRefGoogle Scholar
  114. Nieh JC, Barreto LS, Contrera FAL, Imperatriz-Fonseca VL (2004) Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proc R Soc Lond B 271:1633–1640CrossRefGoogle Scholar
  115. Nunes TM, Nascimento FS, Turatti IC, Lopes NP, Zucchi R (2008) Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim Behav 75:1165–1171CrossRefGoogle Scholar
  116. Nunes TM, Turatti IC, Lopes NP, Zucchi R (2009a) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35:1172–1180PubMedCrossRefPubMedCentralGoogle Scholar
  117. Nunes TM, Turatti IC, Mateus S, Nascimento FS, Lopes NP, Zucchi R (2009b) Cuticular hydrocarbons in the stingless bee Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponini): differences between colonies, castes and age. Genet Mol Res 8:589–595PubMedCrossRefPubMedCentralGoogle Scholar
  118. Nunes TM, Mateus S, Turatti IC, Morgan E, Zucchi R (2011) Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals. Anim Behav 81:463–467CrossRefGoogle Scholar
  119. Nunes TM, Mateus S, Favaris AP, Amaral MFZJ, von Zuben LG, Clososki GC, Bento JMS, Oldroyd BP, Silva R, Zucchi R, Silva DB, Lopes NP (2014a) Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds. Sci Rep 4:7449PubMedPubMedCentralCrossRefGoogle Scholar
  120. Nunes TM, von Zuben LG, Costa L, Venturieri GC (2014b) Defensive repertoire of the stingless bee Melipona flavolineata Friese (Hymenoptera: Apidae). Sociobiology 61:541–546CrossRefGoogle Scholar
  121. Nunes-Silva PN, Imperatriz-Fonseca VL, Gonçalves LS (2009) Hygienic behavior of the stingless bee Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Genet Mol Res 8:649–654PubMedCrossRefPubMedCentralGoogle Scholar
  122. Packer L (2003) Comparative morphology of the skeletal parts of the sting apparatus of bees (Hymenoptera: Apoidea). Zool J Linnean Soc 138:1–38CrossRefGoogle Scholar
  123. Page RE Jr (2013) The spirit of the hive: the mechanisms of social evolution. Harvard University Press, CambridgeCrossRefGoogle Scholar
  124. Page RE Jr, Metcalf RA, Erickson EH Jr, Lampman RL (1991) Extractable hydrocarbons and kin recognition in the honey bee (Apis mellifera L.). J Chem Ecol 17:745–756PubMedCrossRefPubMedCentralGoogle Scholar
  125. Patricio EFLRA, Cruz-López L, Morgan ED (2002) Electroantennography in the study of two stingless bee species (Hymenoptera: Meliponini). Braz J Biol 64:827–831CrossRefGoogle Scholar
  126. Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714CrossRefGoogle Scholar
  127. Pianaro A, Flach A, Patricio EFLRA, Nogueira-Neto P, Marsaioli AJ (2007) Chemical changes associated with the invasion of a Melipona scutellaris colony by Melipona rufiventris workers. J Chem Ecol 33:971–984PubMedCrossRefPubMedCentralGoogle Scholar
  128. Pianaro A, Menezes C, Kerr WE, Singer RB, Patricio EFLRA, Marsaioli AJ (2009) Stingless bees: chemical differences and potential functions in Nannotrigona testaceicornis and Plebeia droryana males and workers. J Chem Ecol 35:1117–1128PubMedCrossRefPubMedCentralGoogle Scholar
  129. Poiani SB, Morgan ED, Drijfhout FP, Cruz-Landim Cd (2014) Separation of Scaptotrigona postica workers into defined task groups by the chemical profile on their epicuticle wax layer. J Chem Ecol 40:331–340PubMedCrossRefPubMedCentralGoogle Scholar
  130. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, PortlandGoogle Scholar
  131. Quezada-Euán JJG, González-Acereto JA (2002) Notes on the nest habits and host range of cleptobiotic Lestrimelitta niitkib (Ayala 1999) (Hymenoptera: Meliponini) from the Yucatán peninsula, México. Acta Zool Mex 86:245–249Google Scholar
  132. Quezada-Euán JJG, López-Velasco A, Pérez-Balam J, Moo-Valle H, Velazquez-Madrazo A, Paxton RJ (2011) Body size differs in workers produced across time and is associated with variation in the quantity and composition of larval food in Nannotrigona perilampoides (Hymenoptera, Meliponini). Insect Soc 58:31–38CrossRefGoogle Scholar
  133. Quezada-Euán JJG, Ramírez J, Eltz T, Pokorny T, Medina R, Monsreal R (2013) Does sensory deception matter in eusocial obligate food robber systems? A study of Lestrimelitta and stingless bee hosts. Anim Behav 85:817–823CrossRefGoogle Scholar
  134. Quezada-Euán JJG, May-Itzá WdJ, Montejo E, Moo-Valle H (2015) Isometric worker size variation in relation to individual foraging preference and seasonal colony growth in stingless bees. Insect Soc 62:73–80CrossRefGoogle Scholar
  135. Raguso RA (2001) Floral scent, olfaction, and scent-driven foraging behavior. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination: animal behavior and floral evolution. Cambridge University Press, Cambridge, pp 83–105CrossRefGoogle Scholar
  136. Rasmussen C, Cameron SA (2010) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc 99:206–232CrossRefGoogle Scholar
  137. Ratnieks FLW, Anderson C (1999) Task partitioning in insect societies. II. Use of queueing delay information in recruitment. Am Nat 154:536–548PubMedCrossRefPubMedCentralGoogle Scholar
  138. Riveros AJ, Groenenberg W (2010) Sensory allometry, foraging task specialization and resource exploitation in honeybees. Behav Ecol Sociobiol 64:955–966CrossRefGoogle Scholar
  139. Robinson GE, Huang ZY (1998) Colony integration in honey bees: genetic, endocrine and social control of division of labor. Apidologie 29:159–170CrossRefGoogle Scholar
  140. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  141. Roubik DW, Smith BH, Carlson RG (1987) Formic acid in caustic cephalic secretions of stingless bee Oxytrigona (Hymenoptera: Apidae). J Chem Ecol 13:1079–1086PubMedCrossRefPubMedCentralGoogle Scholar
  142. Rothenbuhler WC (1964) Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am Zool 12:578–583Google Scholar
  143. Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects, vol III. Academic Press, London, pp 361–423CrossRefGoogle Scholar
  144. Sakagami SF, Zucchi R (1966) Estudo comparativo do comportamento de varias especies de abelhas sem ferrão, com especial referencia oa processo de aprovisionamento e postura das celulas (Comparative study of various stingless bees behaviour with special provitioning reference process and cell posture). Ciencia e Cultura 18:283–296Google Scholar
  145. Sakagami SF, Roubik DW, Zucchi R (1993) Ethology of the robber stingless bee, Lestrimelitta limao (Hymenoptera: Apidae). Sociobiology 21:237–277Google Scholar
  146. Shackleton K, Toufailia A, Balfour NJ, Nasciento FS, Alves DA, Ratnieks FLW (2015) Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees. Behav Ecol Sociobiol 69:273–281PubMedCrossRefPubMedCentralGoogle Scholar
  147. Schmidt VM, Hrncir M, Schorkopf DLP, Mateus S, Zucchi R, Barth FG (2008) Food profitability affects intranidal recruitment behaviour in the stingless bee Nannotrigona testaceicornis. Apidologie 39:260–272CrossRefGoogle Scholar
  148. Schorkopf DLP, Jarau S, Francke W, Twele R, Zucchi R, Hrncir M, Schmidt VM, Ayasse M, Barth FG (2007) Spitting out information: Trigona bees deposit saliva to signal resource locations. Proc R Soc B 274:895–898PubMedCrossRefPubMedCentralGoogle Scholar
  149. Schorkopf DLP, Hrncir M, Mateus S, Zucchi R, Schmidt VM, Barth FG (2009) Mandibular gland secretions of Meliponine worker bees: further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signalling. J Exp Biol 212:1153–1162PubMedCrossRefPubMedCentralGoogle Scholar
  150. Schorkopf DLP (2016) Male Meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight. J Comp Physiol A 202:667–678CrossRefGoogle Scholar
  151. Seeley TD (1985) Honeybee ecology, a study of adaptation in social life. Princeton University Press, PrincetonCrossRefGoogle Scholar
  152. Seeley TD (1995) The wisdom of the hive, the social physiology of honeybee colonies. Harvard University Press, CambridgeGoogle Scholar
  153. Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80CrossRefGoogle Scholar
  154. Septanil MPB, Mateus S, Turatti IT, Nunes TM (2012) Mixed colonies of two species of congeneric stingless bees (Hymenoptera: Apinae, Meliponini) display environmentally-acquired and endogenously-produced recognition signals. Physiol Entomol 37:72–80CrossRefGoogle Scholar
  155. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311CrossRefGoogle Scholar
  156. Smith BH, Roubik DW (1983) Mandibular glands of stingless bees (Hymenoptera: Apidae): chemical analysis of their contents and biological function in two species of Melipona. J Chem Ecol 9:1465–1472PubMedCrossRefPubMedCentralGoogle Scholar
  157. Sommeijer MJ (1984) Distribution of labour among workers of Melipona favosa F: age polyethism and worker oviposition. Insect Soc 31:171–184CrossRefGoogle Scholar
  158. Sommeijer MJ (1987) Age-polyethism in stingless bees and evidence of flexible individual ontogenetic sequences. In: Eder J, Rembold H (eds) Chemistry and biology of social insects. Peperny, München, pp 129–130Google Scholar
  159. Sommerlandt FMJ, Huber W, Spaethe J (2014) Social information in the stingless bee, Trigona corvina Cockerell (Hymenoptera: Apidae): the use of visual and olfactory cues at the food site. Sociobiology 61:401–406CrossRefGoogle Scholar
  160. Spivak M, Downey DL (1998) Field assays for hygienic behavior in honey bees (Hymenoptera: Apidae). J Econ Entomol 91:64–70CrossRefGoogle Scholar
  161. Tofilski A (2002) Influence of age polyethism on longevity of workers in social insects. Behav Ecol Sociobiol 51:234–237CrossRefGoogle Scholar
  162. Toufailia HA, Alves DA, Bento JMS, Marchini LC, Ratnieks FLW (2016) Hygienic behaviour in Brazilian stingless bees. Biol Open 5:1712–1718PubMedPubMedCentralCrossRefGoogle Scholar
  163. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK (ed) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 79–103Google Scholar
  164. van Veen JW (2000) Cell provisioning and oviposition in Melipona beecheii (Apidae, Meliponinae), with a note on caste determination. Apidologie 31:411–419CrossRefGoogle Scholar
  165. van Veen JW, Sommeijer MJ, Meeuwsen F (1997) Behaviour of drones in Melipona (Apidae, Meliponinae). Insect Soc 44:435–447CrossRefGoogle Scholar
  166. van Zweden JS, D’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 222–243CrossRefGoogle Scholar
  167. Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188PubMedPubMedCentralCrossRefGoogle Scholar
  168. Velthuis HHW (1997) The biology of stingless bees. Dept. of Ethology, Utrecht University, UtrechtGoogle Scholar
  169. Velthuis HHW, Cortopassi-Laurino M, Pereboom Z, Imperatriz-Fonzeca VL (2003) The conservative egg of the genus Melipona and its consequences for speciation. In: Melo GAR, Alves-dos-Santos I (eds) Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure. Editora UNESC, Criciúma, pp 171–176Google Scholar
  170. Velthuis HHW, Koedam D, Imperatriz-Fonseca VL (2005) The males of Melipona and other stingless bees, and their mothers. Apidologie 36:169–185CrossRefGoogle Scholar
  171. von Zuben LG, Schorkopf DLP, Elias LG, Vaz ALL, Favaris AP, Clososki GC, Bento JMS, Nunes TM (2016) Interspecific chemical communication in raids of the robber bee Lestrimelitta limao. Insect Soc 63:339–347CrossRefGoogle Scholar
  172. Verdugo-Dardón M, Cruz-López L, Malo EA, Rojas JC, Guzmán-Díaz M (2011) Olfactory attraction of Scaptotrigona mexicana drones to their virgin queen volatiles. Apidologie 42:543–550CrossRefGoogle Scholar
  173. Villa JD, Weiss MR (1990) Observations on the use of visual and olfactory cues by Trigona spp foragers. Apidologie 21:541–545CrossRefGoogle Scholar
  174. Waddington KD (1989) Implications of variation in worker body size for the honey bee recruitment system. J Insect Behav 2:91–103CrossRefGoogle Scholar
  175. Wille A (1979) Phylogeny and relationships among the genera and subgenera of the stingless bees (Meliponinae) of the world. Rev Biol Trop 27:241–277Google Scholar
  176. Wille A (1983) Biology of the stingless bees. Annu Rev Entomol 28:41–64CrossRefGoogle Scholar
  177. Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  178. Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. In: Kinne O (ed) Excellence in ecology. Book 2. Ecology Institute, Oldendorf/LuheGoogle Scholar
  179. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  180. Wyatt TD (2003) Pheromones and animal behaviour. Communication by smell and taste. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  181. Zucchi R (1993) Ritualized dominance, evolution of queen-worker interactions and related aspects in stingless bees. (Hym., Apidae). In: Sakagami SF, Inoue T, Yamane S (eds) Evolution of insect societies. Hakuhinsha, Tokyo, pp 207–249Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • José Javier G. Quezada-Euán
    • 1
  1. 1.Departamento de Apicultura Tropical, Campus de Ciencias Biológicas y AgropecuariasUniversidad Autónoma de YucatánMéridaMexico

Personalised recommendations