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Colony Function and Communication

  • José Javier G. Quezada-Euán
Chapter

Abstract

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

Keywords

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)

    Guard

     
  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

Species

Intensity of defense

Worker populationa

Strategy against mammals

Strategy against insects

Melipona beecheii

Medium

800–1500

Bite, pheromone

Block nest entrance, suicidal bite

Scaptotrigona pectoralis

Intense

2000–4000

Massive attack, bite, recruit more attackers

Suicidal bite

Nannotrigona perilampoides

None

700–1200

Retreat

Resin to immobilize intruders, retreat

Plebeia

None

600–1000

Retreat

Resin to immobilize intruders, retreat

Frieseomelitta nigra

None

500–1000

Retreat

Block entrance, resin to immobilize intruders, retreat

Trigona fuscipennis

Intense

5000–10,000

Massive attack, caustic bite, recruit more attackers

Suicidal bite, resins

Partamona bilineata

Intense

2000–4000

Massive attack, bite

Suicidal bite, resins

Trigona fulviventris

None

500–1000

Retreat

Block entrance, resins

Cephalotrigona zexmeniae

None

500–1200

Retreat

Block entrance, resins

Lestrimelitta niitkib

None

3000–5000

Retreat

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.

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© 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

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