Keywords

6.1 Castes

The origin of the morphological variation that establishes the social role (caste) is one of the definitive elements of the most sophisticated insect societies (Noll and Wenzel 2008). The study of castes differences in Epiponini species in Brazil began with the works of Richards (1978). Among Brazilian authors, studies of Shima et al. (1994, 1996a, b, 1998, 2000) were the pioneers. Understanding the mechanisms that lead to this differentiation is therefore of great importance for understanding the evolution of eusociality (Jeanne and Suryanarayanan 2011). The degree of distinction between breeding and worker caste varieties is often used as part of the definition of the degree of sociality (Noll et al. 2004), with highly social species presenting a complex division of labor, caste morphological differentiation, and a large number of individuals (Bourke 1999).

In Vespidae, this degree of differentiation ranges from no difference in the subfamily Stenogastrinae to large differences in size and morphology in Vespinae (Jeanne and Suryanarayanan 2011). In species presenting distinct morphological castes, the developmental difference between the future queens and workers should begin in the larval stage (Jeanne and Suryanarayanan 2011). In the independent-founding species of Polistinae, although the castes are morphologically identical, they present physiological differences that also should have origin in the larval stage (O’Donnell 1998a). This fact is supported by evidence that differences in mRNA expression and levels of hexameric storage proteins are already evident in the fifth and last larval instar in Polistes metricus Say (Jeanne and Suryanarayanan 2011; Hunt et al. 2007; Toth et al. 2007). In the case of Epiponini species, although described as highly social (Noll et al. 2004), the distinction between caste is not very evident and often difficult to identify (Richards and Richards 1951; Richards 1978, cited as Polybiini, junior synonym of Epiponini, see Carpenter 1993, 1997). According to Jeanne (2003), the complexity in this tribe is more related to the number of behaviors exhibited by the workers than to the presence of morphological differences.

There is no evidence of a genetic basis for caste differentiation in wasps (Jeanne and Suryanarayanan 2011). Differences in size among castes appeared independently in several taxa of this tribe, and caste evolved in different ways in the various lineages of Epiponini (Noll et al. 2004). A phylogenetic interpretation showed several distinct syndromes , representing a more complex scenario than previously thought (Noll et al. 2004; Noll and Wenzel 2008), challenging the defined standards. The four syndromes are (1) absence of caste differentiation (no differences in size or shape associated with reproduction); (2) physiological castes (absence of morphometric differences between castes, but females can be separated by degree of ovarian development); (3) larger queens, but with the same shape; and (4) queens who are different in size and shape from the workers (Noll et al. 2004; Chavarría 2013; Fig. 6.1 and Table 6.1).

Fig. 6.1
figure 1

The four syndromes related to the determination of castes in Polistinae. In (a, b) castes do not present morphological differences in size or shape. However, in (b) females can be separated by the degree of development of the ovaries (physiological caste). In (c) queens are larger in size, but there is no difference in the shape, and in (d) queens differ in size and shape from workers. The crowns identify the reproductive caste (queens)

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Table 6.1 Epiponini Differences between castes related to morphology and the presence of intermediates in
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As expected for highly social insects, pre-imaginal determination, given by nutritional differences during larval development (Hunt et al. 1996; Sakagami et al. 1996) or changes in the longitudinal axis of the body due to different programs in developmental parameters in the pre-adult stage (Jeanne et al. 1995), has been reported for the genera Agelaia (Fig. 6.2), Apoica, Chartergus, Polybia, Protopolybia, and Pseudopolybia (Noll et al. 2004). On the other hand, breeding females in Chartergellus, Metapolybia, Parachartergus, and Synoeca are morphologically similar to non-breeding and present no physiological discontinuities. In these cases, castes are flexible, and the determination is imaginal, given by the disputes between adult females instead by larval manipulation (West-Eberhard 1981; Mateus et al. 2004; Noll and Wenzel 2008; Chavarría 2013). Theoretically, in species with imaginal determination, all females when emerging could develop the ovaries and reach the status of queen, a condition that could lead to conflicts among the individuals of the colony, since the workers could also lay eggs (Hart and Ratnieks 2005).

Fig. 6.2
figure 2

Queen (a) and worker (b) of Agelaia pallipes (Olivier), species that presents a clear morphological difference between the castes

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In fact, in many colonies, workers with functional ovaries (named intermediates by Richards and Richards 1951) have been identified. The role of intermediate is debatable, being considered as producers of trophic eggs, males (Richards 1971), or even young queens (Forsyth 1978; West-Eberhard 1978; Gastreich et al. 1993). The level of ovarian development is inversely proportional to the number of queens, that is, when a few females are present, the intermediates present more developed ovaries (Fig. 6.3) and vice versa (Richards 1971; West-Eberhard 1978). Nevertheless, intermediates are absent in many other taxa (revised in Noll et al. 2004). Anyway, the presence of this type of female is part of a complex scenario related to the evolution of castes (Noll 2013).

Fig. 6.3
figure 3

Different degrees of ovarian development in Epiponini. Pictures of Protonectarina sylveirae (de Saussure). (a) Worker, (b) queen, and (c) intermediate

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The origin of queens that are highly tolerant of each other brings some consequences. The first is that many females could aspire for a chance of reproduction, which would lead to the totipotency of the caste (Strassmann et al. 2002). As a consequence, it would be expected to find a generalized ovarian development in members of polygynic societies, and, in fact, in several Epiponini species, workers who lay eggs are found (Noll et al. 2004). Several basal genera of Epiponini fit into the proposed scenario for polygynic groups (West-Eberhard 1978, 1981), that is, caste flexibility due to the absence of morphological differences between them and ovarian development in all females. This condition is found mainly in Angiopolybia, Pseudopolybia, Parachartergus, Chartergellus, and Leipomelles (Noll et al. 2004). Thus, the distribution of this characteristic (presence of workers laying eggs) actually constitutes a plesiomorphic rather than an apomorphic state (Noll 2013).

Due to the absence of morphologically distinct castes, the social way of life in Epiponini has already been considered as little complex. However, Jeanne (2003) suggested the presumption of self-organization rather than the presence of distinct morphologies as a characteristic that would define complex societies. In this case, the presence of self-organization would remove the need for evolution in two distinct forms in Epiponini (Noll 2013). Indeed, as suggested by West-Eberhard (2003), the origin of morphologically distinct castes is much more a condition for colony stability and defense than indicative of social complexity. From this perspective, the complex Epiponini societies may have undergone a phase of totipotent and monomorphic females for several morphologically distinct queen systems in different lineages. Such a theory proved to be perfectly congruent when optimized in a cladogram of Epiponini genera (Noll et al. 2004).

Reproductive control in social wasps can be done in two ways: through physical aggression (primitively eusocial wasps) or through chemical control. Within the colonies of primitively eusocial wasps (Polistes, Mischocyttarus, Belonogaster, Parapolybia, and Ropalidia), there is a hierarchy of dominance, where the female with greater ovarian development is solely in charge of egg laying (Fletcher and Ross 1985). Because any female can lay eggs, the queen status is maintained within the colony through physical aggression and oophagy. In Polistes , dominance interactions are more frequent than in Mischocyttarus (Spradbery 1991), and, in Ropalidia there is little or no direct interaction, with this genus presenting the least dominance repertoire among Polistinae wasps (Spradbery 1991; Kardile and Gadagkar 2002; Bhadra et al. 2010). After establishment of dominance, a reduction in the levels of aggression is observed (West-Eberhard 1986; Hughes et al. 1987), suggesting that the reproductive dominance can also be maintained by chemical signals (West-Eberhard 1986; Dapporto et al. 2007; Bhadra et al. 2010), possibly by mixtures of hydrocarbons secreted by the Van der Vecht gland (Dapporto et al. 2007). The factors of endocrine control and oogenesis are not yet clear, however. Dominance behavior alone seems to be insufficient to maintain reproductive control (Röseler 1991). In the absence of the original queen, one of the female co-founders of the nest or the female presenting the highest ovarian development may assume a role in reproduction (Spradbery 1991). The queen monopolizes the production of eggs but can also forage occasionally and starts the construction of new cells (Chavarría 2013).

For Epiponini, physical aggression was observed only during the phase of establishment and selection of queens (Mateus 2005); however, physical aggression on the part of the queen against the workers, to maintain their status within the colony, is not common. For this reason, it is believed that reproductive control is also made through chemical signaling or hormonal control (Naumann 1970; Forsyth 1978; Fletcher and Ross 1985; West-Eberhard 1989a; Spradbery 1991), although no study has proven this phenomenon. In addition to chemical signals, queens use ritualized postures to communicate their status within the colony (West-Eberhard 1978; Spradbery 1991). The queens, in Epiponini, do little more than lay eggs and perform no other task in the colony (Herman et al. 2000).

If the queens in Epiponini do not exercise a strong reproductive control, the workers do. The workers test and remove queens from the colony (West-Eberhard 1978, 1981; Herman et al. 2000; Platt et al. 2004) and favor the production of queens in colonies where there is a low number of queens and the production of males in colonies with high number of queens (Queller et al. 1993). Moreover, workers favor production of males by queens because they are more genetically related to the “sons” of the queens than to the “sons” of other workers (Hastings et al. 1998), which seems good to maintain the “workers’ interest” (Strassmann et al. 1997, 1998). This type of control is probably done in species with imaginal determination, although other control mechanisms may be related (Chavarría 2013). Studies in colonies of Protopolybia sedula (de Saussure) (Naumann 1970, still as P. pumila in his works), Metapolybia aztecoides Richards (West-Eberhard 1973, 1978), Parachartergus colobopterus (Lichtenstein) (Herman et al. 2000), Asteloeca ujhelyii (Ducke) (Nascimento et al. 2004), Parachartergus fraternus (Gribodo) (Mateus 2005), and Metapolybia docilis Richards (Chavarría 2009) demonstrated that worker behavior may be an important component in the mechanism of delimitation of functions in the colony.

A peculiar feature that occurs in Polistinae is the presence of polygyny (presence of several queens coexisting in the same nest). This characteristic appeared three times within the subfamily – in the genera Polybioides and Ropalidia, and in the tribe Epiponini (Carpenter 1991) – and is associated with the colony’s foundation mode by swarming (the colony is constructed by a large number of workers accompanied by more than one queen) and complex social organization (Carpenter 1991; Jeanne 1991; Fig. 6.4). Epiponini species may exhibit permanent polygyny or variation in queen numbers (decrease) during the colony cycle, resulting in monogyny (West-Eberhard 1978; Richards 1978; Jeanne 1991). The presence of polygyny in the most basal clades indicates that the presence of multiple functional queens was already present in the common ancestor of the tribe (Carpenter 1991; Noll 2013).

Fig. 6.4
figure 4

Evolution of polygyny in Epiponini. (a) In a plesiomorphic society with short-term monogyny, the dominant female is intolerant of the reproduction of other females. The queen performs policing, while the workers are tolerant to the reproduction of other females. Occasionally, the workers reproduce. (b) In Epiponini no intolerant queens are present; instead, reproduction is performed by several tolerant females. The role of policing is adopted by workers, who suppress each other, as well as select among breeders. (Modified from Noll 2013)

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It is not difficult to imagine that the origin of polygyny was molded by the same factors as swarm foundation and nest architecture and that ant predation was an important factor (Jeanne 1979). There is a consensus that eusociality of wasps originated in the tropics (Evans and West-Eberhard 1970), where ants are the most important predators of the colonies (Richards and Richards 1951). From this point of view, it is appropriate to state that the most peculiar characteristics of the Epiponini lifestyle are the result of the improvement of defense against ants (Richards 1971, 1978; Jeanne 1975, 1991; Starr 1990; Simões et al. 1996). Thus, the rapid abandonment of the nest through the migratory behavior (swarming) would be an important strategy, assured by polygyny, that led to the selection of queens morphologically undifferentiated (less body mass, easier to fly) and numerically more abundant (greater opportunity for reestablishment of the colony in a new place) (Mateus 2005). Considering that the loss of a single queen could be fatal, the presence of several queens could be advantageous for the colony in terms of survival (Noll 2013).

The presence of several queens laying eggs could represent a problem regarding “conflict of interest” occurring in the colonies of social insects (Noll 2013). Although degrees of relatedness may be low in colonies of the independent-founding wasps Polistes (Pickett et al. 2006), an additional problem arises in Epiponini: the division of reproduction among several queens would result in an even lower degree of kinship among the females of one colony (Hastings et al. 1998), which would not reinforce the sterility of the workers. However, kinship analyses for Epiponini colonies have indicated that the degree of relationship between females is relatively high (Queller et al. 1988, 1993; Strassmann et al. 1992; Gastreich et al. 1993; Hughes et al. 1993; Hastings et al. 1998). These results are in line with what West-Eberhard (1978, 1981) observed in colonies of Metapolybia aztecoides . After the swarm, at the beginning of the cycle, several queens and workers are present. Throughout the development of the colony, some of the queens disappear or begin to display worker functions, and, later, the number of queens is reduced until there remains a few or only one. Queen production and swarms occur predominantly after the establishment of monogyny or oligogyny, restricting the production of future queens to only a few individuals. This pattern is observed in several other species, such as Polybia occidentalis (Olivier) (West-Eberhard 1978; Queller et al. 1993), Parachartergus colobopterus (Strassmann et al. 1991), Polybia emaciata Lucas (Strassmann et al. 1992), Protopolybia exigua (de Saussure) (Gastreich et al. 1993), Brachygastra mellifica (Say) (Hastings et al. 1998), and Agelaia multipicta (Haliday) (West-Eberhard 1990). The term cyclic oligogyny was coined to define the decrease in the number of queens and the production of new ones during the period when there are few of them in the colony. That way, the relationship between the queen and daughters is increased, as predicted by the kinship selection theory (Hamilton 1964a, b, 1972). The high kinship is also maintained by the fact that queens in Epiponini are inseminated only once (Goodnight et al. 1996). The possibility that the wasps of this tribe are inflexible in terms of loss of these elements of sociality should not be ruled out either (Noll 2013).

6.2 Communication

6.2.1 Alarm Pheromone

Swarm-founding wasps and their populous colonies are engaged in sophisticated communication systems to coordinate the activities of all members of the colony (Jeanne 1991). The defense behavior in Polybia occidentalis involves two steps. First, in response to a sudden movement or mechanical disturbance to the nest, a large number of individuals are quickly recruited to the outer surface of the envelop. Second, a number of these individuals immediately fly and attack the intruder or predator. Alarm recruitment has been demonstrated experimentally in Polybia occidentalis (Jeanne 1981, 1991). The workers’ venom contains a pheromone that immediately recruits a large number of adults, which move to the surface of the envelope. Outside the nest, the attack occurs immediately against dark-colored objects that move close to the nest. The chemical alarm communication certainly occurs in most of the swarming wasps, but it is still necessary to investigate whether it occurs in colonies with low numbers of individuals (Jeanne 1981, 1991). The alarm and defense behavior of the nest in Synoeca surinama (Linnaeus) is coordinated by visual factors and by odors, which are recognized by the individuals of the same colony. In the presence of intruders, these factors together incite and produce the wasp attack (Castellón 1981).

6.2.2 Chemical Communication During Migration

Communication during migration depends on the chemical signals left by the scout workers on different substrates indicating a direction to follow (Naumann 1975; Jeanne 1975; Forsyth 1978; West-Eberhard 1982; Mateus 2005; Mateus 2011). For migration to occur, three major challenges need to be overcome. First, the scouts select a location for the construction of the new nest. Second, these workers create a “trail” of chemical signals, left on prominent objects (such as leaves) along the way to the new site. Finally, the rest of the colony follows the chemical trail to reach the site of the new nest (Sonnentag and Jeanne 2009; Mateus 2011).

The chemical communication during swarming in Epiponini seems to be related to a gland present in the fifth gastral sternite. Reports of the presence of this gland were made by Richards (1971) and later studied by Jeanne and Post (1982) and Jeanne et al. (1983). The “dragging behavior”, which consists of rubbing the gaster on a substrate to make the chemical pathway that is followed by the rest of the colony during migration, was first described by Naumann (1975) and observed in species of the genera Agelaia, Angiopolybia, Leipomeles, and Polybia. Jeanne (1975, 1981) experimentally confirmed the findings of Naumann (1975) observing the wasps followed an artificial trail made with substances removed from the gland of the fifth gastral sternite. However, this seems not to be the only strategy used. Studies with Apoica pallens (Fabricius) (Howard et al. 2002) showed a different strategy of chemical communication during the swarm. This species does not make a chemical trail on a substrate and does not previously select the location of the new nest. After leaving the old nest, the population forms clusters in leaves of plants, and the recruitment is done when the wasps elevated the abdomen and exposes the base of the fifth and sixth sternites. This behavior suggests that the wasps are emitting a pheromone in the air (“calling display”) to group the population and lead it to a site to build the new nest (Howard et al. 2002).

In Parachartergus fraternus , although the presence of scouts doing “dragging behavior” during migration has been observed by some authors (Jeanne et al. 1983; Smith et al. 2002), no evidence of external glands was found in the gastral sternites (Jeanne et al. 1983). In this species, the communication of the end point of the chemical pathway was established by dozens of scouts, creating an area of easy recognition due to the strong odor of the substance applied to the substrate. In the moments that preceded the migration, it was observed that the number of scouts sprinkling venom on the substrate of the new nest site is high. Simultaneously, in the old nest, the scouts who returned there make lateral movements with the abdomen (“dragging behavior”) in the substrate and oral contacts to signal and stimulate the population to migrate. The strategy of marking the place of the new nest by sprinkling venom possibly prevents the action of possible predators until the colony is established (Mateus 2005, 2011). Venom spraying is well known in the Parachartergus (Jeanne et al. 1995; West-Eberhard 1982), which has specialized muscles in the venom reservoir (Maschwitz and Kloft 1971). Chemical communication during migration in the Epiponini has been described as very efficient, since the loss of individuals during the process has been reported as low. The main causes of loss are related to predation or to the fact that individuals are newly emerged and not fully capable (Bouwma et al. 2003; Mateus 2011).

There are two distinct types of migration in Epiponini, “diffuse swarms” and “clumped swarms”. For both types, use of chemical communication as a signal of the path to the new nest was observed for all species studied (West-Eberhard 1982). In diffuse swarms, observed in Agelaia areata (Say) (Jeanne 1975), Synoeca surinama (West-Eberhard 1982), and Parachartergus fraternus (Mateus 2011), the wasps spread over an area of more than 100 m in length by 20–50 m in width, in search of the chemical track. In the clumped swarm, several clusters are formed on a migration route, and, as the population advances along the migration path using the chemical trail, the clusters disintegrate behind the advance (West-Eberhard 1982). This type of migration was observed in Parachartegus apicalis (Fabricius), Polybia ignobilis (Haliday), Polybia raui Bequaert, Polybia occidentalis (Forsyth 1981), and Polybia sericea (Olivier) (Jeanne 1981).

6.2.3 Recruitment for Food Forage

Wasps can be considered as the great flying hunters and gatherers of the world of social insects. As far as we know, all social wasps are omnivorous, feeding on both animal proteins and sugar-rich carbohydrate sources. The sources of foraged proteins are predominantly living arthropods, which provide nutrients for immature growth. Carbohydrate sources serve primarily as an energy source for adults (Jeanne and Taylor 2009). Unlike other social Hymenoptera, bees and ants, in wasps there is no sophisticated communication system to inform nest mates of location of the source or when and where to forage for food. Thus, the foragers of social wasps seem to act individually (Jeanne and Taylor 2009).

Some hypotheses have been suggested by Jeanne et al. (1995). One is that wasps do not have sufficient genetic variability to give rise to structures or behavior to inform nest mates about the location of resources, which seems unlikely. Swarm-founding wasps exhibited sufficient genetic variability for the evolution of trail pheromones, which guide swarms to new nests (Jeanne 1981, 1991), a mechanism that should probably be able to function in the recruitment of nest mates to food sources. The lack of a signal-based recruitment system may be due also to a social constraint. A critical colony size may be necessary for the benefits of recruitment to outweigh the costs (Beckers et al. 1989), and it can be argued that the number of foragers in most social wasp species is too low to effectively defend food sources against competitors such as some species of ants and stingless bees. A third possibility is that ecological factors may make recruitment an unproductive strategy in social wasps. For recruitment to be worth it, the resources need to be clustered in space and persist for considerable periods of time. However, according to Jeanne and Taylor (2009), it may be premature to generalize that all social wasps do not recruit for food sources, since only a few species have been studied carefully and there are many other species to be studied.

6.2.4 Division of Labor

The division of labor is a central theme in the study of social insects (Garcia and Noll 2013). The ecological success of these groups can be credited to their ability to coordinate their colonies for feeding, breeding, cleaning, and nesting (Beshers and Fewell 2001; Wilson 1979; Wilson and Hölldobler 2005). In ants and termites, the division of labor among castes is regulated by ontogenetic and physiological mechanisms (Miura 2005). In Epiponini, as in bees, the division of labor is associated with age polyethismFootnote 1 and specialization of tasks (Chavarría and Noll 2013; Garcia and Noll 2013).

Workers of independent foundation species begin to forage at the age of several days and combine foraging activities with activities within the nest throughout their lives. Foragers bring food (nectar and prey) and material (vegetable matter and water) to build the nest, and division of labor among them may occur by preference for a particular type of activity (polyethism) and in the way of processing the load (division of tasks). The forager can perform all the necessary handling alone or divide its load of material totally or partially with other members of the colony. The frequency of load partitioning increases with colony growth (Post et al. 1988; Rusina 2006), and the food division is often more frequent than the construction material division (Rusina et al. 2011). In Polistes fuscatus (Fabricius), for example, three functional groups are present: (1) workers who prefer to hunt than to build and tend to pass protein to other individuals, (2) workers who deliver construction material and do not pass prey to other workers, and (3) non-forage workers who engage exclusively in activities within the nest (Post et al. 1988). A similar pattern was found for P. dominula (Christ), P. nimpha (Christ), and P. gallicus (Linnaeus). In the latter two species, however, the constructors were involved in establishing and maintaining the dominance structure of the workers (Rusina 1999, 2006). Dominant workers in Mischocyttarus mastigophorus Richards collect building material and obtain protein food from prey forage more frequently than subordinate individuals (O’Donnell 1998b).

In Epiponini, the high level of social organization resulted in the presence of age-related polyethism and in the specialization of foragers. Handling of the delivered material (building material, water, prey, and nectar) is divided into two sub-tasks: collection and use. Foragers of the two functional groups bring food (prey and nectar) and construction material (wood pulp and water) to the nest and pass to other workers. A forager can deliver a specific type or both types of material throughout its active period. If a forager changes to a different type of load, the change usually occurs within the same group (food or nest material) (Rusina et al. 2011). Construction activity in these wasps is not only subdivided into delivery of pulp and construction but also involves the transportation of water by specialized workers. In addition, pulp delivered by foragers is generally too large to be used directly in the construction, so they have to pass at least part of the material to the workers in the nest who then distribute the material among themselves (Jeanne 1986; O’Donnell and Jeanne 1990; Karsai and Wenzel 1998). According to Jeanne (2003), the main difference between the independent and swarm-founding species is in the way of dealing with the material collected and in the fact that the foragers transfer the material to another worker (and continue to forage), allowing the development of the age polyethism and a more complex organization of the colony. In general, young workers perform tasks within the nest, such as cleaning and caring for the offspring. Meanwhile, the middle-aged workers are concerned with the construction and repair of the nest. Older workers, in turn, act as foragers, carrying material for construction and water and food for the colony, in addition to defending the nest (O’Donnell 2001). Studies with Polybia, Protopolybia, and Agelaia found that young and middle-aged workers perform tasks in the nest such as construction, care of the offspring, nest maintenance, and defense, while older workers forage (Simões 1977; Forsyth 1978; Jeanne et al. 1988, 1992). Chavarría and Noll (2013) observed a similar number of young and old female workers performing tasks such as cell inspection, construction, and foraging in Metapolybia miltoni Andena and Carpenter colonies. However, younger workers tend to forage less than the older ones (Chavarría and Noll 2013).

Specialization , that is, the presence of workers who perform a single type of task, is rare in most social wasps (Robinson 1992; Sendova-Franks and Franks 1999; O’Donnell 1998c; Karsai and Wenzel 2000; Beshers and Fewell 2001; Johnson 2003). Karsai and Wenzel (2000) did not find specialization in colonies of Metapolybia aztecoides and M. mesoamerica Smethurst and Carpenter. The same was observed by Chavarría and Noll (2013) for Metapolybia miltoni. Mateus (2005) also found flexibility in performing tasks in Parachartergus fraternus, where a worker who acted as a scout during the pre-swarm was subsequently observed laying eggs and, when dissected, the presence of ovaries developed with mature oocytes was found. Other scouts of the same nest performed construction tasks after nest establishment (Mateus 2005). In Polybia occidentalis and Metapolybia sp., there was greater stability in the preference for collection of a type of material when colonies were large (Jeanne 1986; Karsai and Wenzel 1998, 2000). Data obtained for Polybia aequatorialis (Zavattari) indicate that workers with specialization for the same activity have a close genetic relationship (O’Donnell 1996, 1998c). When there is little variation of age in the population, the workers should be allocated to tasks according to the needs of the colony, not being very relevant to the age of the individuals (Chavarría and Noll 2013). On the other hand, in colonies with individuals of different ages, polyethism seems to be more important in the delimitation of tasks, as demonstrated in the works of Jeanne et al. (1988, 1992). In short, the workers’ choice of task depends on the circumstances of the colony, and the workers can be allocated to this or that task according to need (Karsai and Wenzel 2000).

Workers in any insect society retain some degree of behavioral flexibility, which is decisive for the survival of the colony in changing situations (Robinson 1992). Likewise, caste flexibility is an important factor for colony survival in the swarm-founding wasps, allowing these insects to respond efficiently to changes that may occur (Chavarría and Noll 2013). As evidenced by Noll and Wenzel (2008), cast dimorphism evolved at least eight times in Epiponini, and social organization derives directly from an ancestor with incipient caste dimorphism in most taxa. Given this fact, general patterns are insufficient to explain the different strategies adopted by the species of this tribe (Beshers and Fewell 2001; Chavarría and Noll 2013).

6.2.5 Colony Defense

“I suspect that social wasps pay much more attention to ants in their environment than we think”. The phrase by Jeanne (1991) reinforces the idea that in the tropics, the ants represent the most important predators of the colonies of social wasps (Richards and Richards 1951). Predation by these insects may have strongly influenced the evolution of these wasps (Jeanne 1979). The rapid abandonment of the nest and swarm, the complex architecture of nests, and the presence of breeds without clear morphological differences suggest evolutionary adaptations against ant predation as well as optimization of work (Jeanne 1975; Wenzel 1998). While independent-founding species (Polistes and Mischocyttarus) rely heavily on secreted chemical repellents to keep ants away from their offspring, the swarming wasps depend primarily on the envelope surrounding the combs, coupled with the presence of workers guarding the nest entrance (Jeanne 1975). In addition, in the face of an ant attack, abandoning the nest by the rapid migration of the adult population is certainly an important and unique strategy in Epiponini (Mateus 2005).

In addition to envelope protection, workers actively guard the nest (Jeanne 1975, 1991). When the ants get too close, the wasps can resort to a series of behaviors to drive away the invaders. Protopolybia exigua and Polybia occidentalis, for example, exhibit “wing buzzing” and “burst” behaviors, where female workers swing their bodies up and backward by buzzing their wings rapidly and producing a snap (Chadab 1979). In P. exigua, this behavior is shown when visual or olfactory stimuli, as well as the odor of formic acid, are detected by the wasps and act as a warning signal to the companions who can quickly evacuate the nest if the ants reach this one (Chadab 1979). When an ant reaches a P. occidentalis nest, it can be stung by a worker who immediately uses the jaws to trap and carry the ant away from the nest (Jeanne 1991). As described by Chadab (1979), buzzing and burst behaviors cause small bursts of air directed at the ants whose antennae curve at each flight wrist. These pulses paralyze the ants momentarily, and the display of these behaviors persistently by the wasps results in the retreat of the ants (Jeanne 1991). Workers of Clypearia sulcata (de Saussure), Metapolybia aztecoides, and Polybia occidentalis use the jaws to scrape the substrate of the nest where the ants passed in order to remove the pheromone trail left by them (Chadab 1979; West-Eberhard 1989b; Jeanne 1991). Thus, the chances of ants reaching the nest in the future are reduced (Jeanne 1991).

Although most species bet on the active defense of the nest against invasive ants, a different strategy has evolved in some species. Nectarinella xavantinensis Mateus and Noll, N. championi (Dover), and Leipomelles dorsata (Fabricius) protect access to the nest with the placement of “sticky pillars” in areas near the entrance of the nest, apparently produced from an oral secretion (Jeanne 1991; Wenzel 1991; Mateus and Noll 1997; Carpenter and Marques 2001). Wasps of these species are quite small, and defending the nest actively against many ant species would be impossible (Jeanne 1991). Envelope protection, active defense, and building sticky traps can be very effective against small ants, but they are not enough against a group of ants, in particular the army ants. The majority of social wasps seem to have no effective defense against army ants, and the tactic against their arrival is the immediate abandonment of the nest by the entire adult population so that they do not end up as prey of the invaders, which will occur with the abandoned larvae and pupae (Jeanne 1991). In some species of Polistinae, however, ways of escaping of predation by these ants have evolved. One of them is to build very high nests in the canopy, as do Agelaia areata, Epipona tatua (Cuvier), and Chartergus metanotalis Richards (Jeanne 1991; Carpenter and Marques 2001). Other species with more resistant envelopes like Synoeca septentrionalis Richards, S. chalibea de Saussure, Polybia emaciata, and P. jurinei de Saussure prevent the entry of army ants using the body itself to block the entrance of the nest.

Curiously, despite the antagonistic relations between the ants and the social wasps, some species developed interspecific associations. Polybia rejecta (Fabricius), a very aggressive social wasp, often builds its nest in association with colonies of the ant Azteca (Richards 1978; Somavilla et al. 2012). This association may be one of the few defenses that tropical wasps have against invasions by ants of the army ants (Richards and Richards 1951). Similarly, wasps exhibit aggressive behavior when the ant colony is disturbed, protecting the ants primarily against predatory mammals such as anteaters (Virgínio et al. 2015). Synoeca chalybea can also construct nests in association with ants of the genus Azteca (Souza et al. 2013).

In addition to barring the ants, the presence of the envelope also seems to be an effective defense against parasites. When these are found, they are far less numerous when compared to the large infestations that may occur in non-enveloped nests of independent-founding species. Forsyth (1978) analyzed 141 colonies of Metapolybia azteca and Polybia occidentalis finding parasites in only 7% of them and less than 1% of offspring infestation. On the other hand, Nelson (1968) observed that about 60% of the colonies of Polistes metricus analyzed by him were parasitized by the moth Chalcoela iphitalis, with some nests reaching 90–95% infestation of the offspring.

The most famous defense mechanism of social wasps is undoubtedly the painful sting. In spite of the bad reputation, the sting apparatus in its origin has as primary function the capture of prey (Macalintal and Starr 1996). However, they assumed an important defense role against bigger enemies, especially in social lineages (Macalintal and Starr 1996). The behavior of stinging would have evolved due to the predation pressure exerted by vertebrates attracted by the increase in colony size, particularly in the tropics, in open and seasonally dry forests (Starr 1985; Carpenter and Marques 2001). This form of defense is undoubtedly quite effective in discouraging potential predators, although, it is not uncommon for wasp colonies to be attacked by vertebrates such as birds, bats, and primates (Jeanne 1975, 1991). Nevertheless, different mechanisms were adopted by other species in an attempt to minimize the risk of being attacked by these animals. Species with small colonies construct nests camouflaged for the purpose of hindering the visualization by vertebrates and parasites. Leipomeles dorsata, for example, constructs its nest at the bottom of a broad leaf and covers the envelope with green details in order to mimic plant venation (Williams 1928; Richards 1978; Jeanne 1991). Other species build large and sturdy nests, inaccessible to most vertebrates.

In Apis mellifera Linnaeus, defense and foraging activities are carried out by different groups of workers (Breed et al. 1990), that is, the workers who act in the defense of the colony are specialized in this task. In Epiponini, Jeanne et al. (1992) analyzing colonies of Polybia occidentalis did not find a subgroup of specialized workers in this task, concluding that the wasps that defended the nest also performed other activities inside the nest and of foraging, for example (Fig. 6.5a). In fact, there is a positive correlation since forager workers are more likely to act in defense than non-forager ones (Jeanne et al. 1992). Still for P. occidentalis, the likelihood of a wasp displaying defense response increases significantly among workers aged between 8 and 12 days, stabilizing after the 13th day (Jeanne et al. 1992; Fig. 6.5b). During a mechanical stimulus, young wasps also leave the nest in response to the attack signal, but only the older workers effectively attack the intruder. This fact makes it clear that the behaviors of “leaving the nest” and “attacking” represent different responses (Jeanne et al. 1992) and that the participation of a large number of individuals in the exit response suggests that this behavior functions as an aposematic sign to the predator (Jeanne et al. 1992).

Fig. 6.5
figure 5

Defense behavior according to age. (a) Frequency of task performance according to the age of the worker. Number of tasks related to nest maintenance, foraging trips, and defensive responses. (b) Frequency of task performance as a function of relative age (age is relative to the transition of each individual from the work in the nest to the foraging). (Modified from Jeanne et al. 1992)

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Thanks to its defensive potential, the sting apparatus is considered a key factor that favored the origin of social behavior several times within Aculeata. Added to this is the fact that only females act as workers in the societies of wasps, bees, and ants (Silveira and Silveira 1994). An evolutionary analysis of the sting apparatus in Vespidae showed that some variations in the characteristics of this structure are related to the highly social way of life (Silva et al. 2014). In addition to the defense function, the use of the sting apparatus in a phylogenetic reconstruction supports the unique origin of eusociality , which would have occurred in the ancestor of Vespinae + Polistinae (Silva et al. 2014).

6.3 General Conclusion

The peculiar features presented by Neotropical social wasps, specially the swarm-founding Epiponini, resulted in a great diversity of species. Among the representatives of this tribe, all stages of caste differentiation are present, from castes morphologically very distinct to forms in which there are no external differences. Physiological differentiation also follows this rule, giving rise, in some species, to females with ovary developed but not fertilized, so-called intermediates. Because of polygyny, many females are able to lay eggs, tolerating each other, and the egg layers are tested and occasionally removed by sterile workers. Chemical communication guides the swarms and defense of the nest, and the tasks performed inside and outside the nest are divided according to the age of the wasps.