Fighting ability and the toxicity of raiding pheromone in an obligate kleptoparasite, the stingless bee Lestrimelitta niitkib

Abstract

The evolution of obligate kleptoparasitism, the theft of food, has led to remarkable innovations, including physical weapons and chemical signals that can evolve into chemical weapons. Stingless bees in the genus Lestrimelitta are excellent examples of this phenomenon because they are obligate kleptoparasites that no longer collect floral resources and instead steal brood resources from other bees. Their ability to raid successfully is thus essential to their fitness even when they fight species that are physically bigger, have larger defense forces, or both. We conducted morphometric analyses, quantified Lestrimelitta niitkib mandibular gland pheromone (MGP) components, and carried out individual fighting trials between L. niitkib and the stingless bee Scaptotrigona mexicana, a common victim species, to shed light on the detailed reasons for their success at robbing. Measurements showed that L. niitkib mandibles have thicker exoskeleton cuticles and overall greater width, particularly in the medial and proximal sections, than S. mexicana, which is quite similar in body size. In all fights, L. niitkib bit victims and released MGP, as it does during raids. Scaptotrigona mexicana victims exhibited significantly increased uncoordinated behaviors and showed partial or complete paralysis. We analyzed and quantified the major components of MGP, which consisted of large quantities of geranial (mean of 253 μg) and neral (48 μg) per bee. Microinjections of 1 bee equivalent (BE) of natural or synthetic MGP and ≥ 0.1 BE of geranial significantly increased deleterious behaviors and paralysis as compared to control injections. We suggest that the large quantities of MGP used during raiding have led to an unexpected outcome, a semiochemical evolving the additional function of a toxin, and contribute to the ability of Lestrimelitta to rob its victims. Significance statement Kleptoparasites, organisms that steal food resources, employ multiple physical and chemical tools to survive. The success of kleptoparasitism requires a balance between honesty and coercion in interspecific communication. The genus Lestrimellita consists of a group of kleptoparasitic stingless bee species that raid other bee colonies for food and therefore depend upon winning these raids. However, why they succeed remains not fully understood. We studied differences in morphology between L. niitkib and its victims, the pheromones they release during raids, and ran individual fight trials between L. niitkib and a common victim to identify why they are successful. We suggest that the release of pheromones at the beginning of raids, in concert with the pheromone’s toxicity, has been combined to improve L. niitkib’s ability to successfully rob.

Investigating the molecular basis of cleptobiosis in eusocial stingless bees (Apidae: Hymenoptera)

“…Queens of Lestrimelitta have a higher number of ovarioles per ovary (10)(11)(12)(13)(14)(15) than most stingless bees (~4) (Sakagami 1982), enabling the production of a larger number of workers. Moreover, the robust mandibles of the Lestrimelitta workers (Nogueira-Neto 1997; James et al 2022) help them overcome the colony defenses of host species.…”

“…Queens of Lestrimelitta have a higher number of ovarioles per ovary (10-15) than most stingless bees (∼4) (Sakagami 1982), enabling the production of a larger number of workers. Moreover, the robust mandibles of the Lestrimelitta workers (Nogueira-Neto 1997; James et al 2022) help them overcome the colony defenses of host species. An important behavioral adaptation of Lestrimelitta and Cleptotrigona species is their foraging strategy, they carry out organized robbing raids in which several individuals simultaneously attack colonies of other species; in C. cubiceps the number of individuals participating in these raids may reach a few dozen (Portugal-Araújo 1958), while in Le-strimelitta it can exceed several hundred (Sakagami et al 1993).…”

“…An important behavioral adaptation of Lestrimelitta and Cleptotrigona species is their foraging strategy, they carry out organized robbing raids in which several individuals simultaneously attack colonies of other species; in C. cubiceps the number of individuals participating in these raids may reach a few dozen (Portugal-Araújo 1958), while in Le-strimelitta it can exceed several hundred (Sakagami et al 1993). Raiding recruitment in Lestrimelitta has been reported to involve the use of semiochemicals (Blum 1966; Sakagami et al 1993) that have toxin functions (James et al 2022), and may also play a role in the host response to raids (von Zuben et al 2016; James et al 2022). Likewise, in an apparent strategy of chemical deception, it has been suggested that Lestrimelitta may share cuticular hydrocarbons with their preferred host species to better conceal their presence (Vázquez et al 2022).…”

Olfactory Strategies in the Defensive Behaviour of Insects

“…A recent study suggests that evolution can also take the reverse path: the stingless bee Lestrimelitta niitkib , which specializes in raiding other species, produces unusually high amounts of common mandibular alarm pheromone compounds. Such a high dose of these compounds, injected through biting, is toxic to bees of similar sizes, thus conferring a fighting advantage to L. niitkib [ 24 ].…”