Changing of the guard: mixed specialization and flexibility in nest defense (Tetragonisca angustula)

Abstract

Task allocation is a central challenge of collective behavior in a variety of group-living species, and this is particularly the case for the allocation of social insect workers for group defense. In social insects, both benefits and considerable costs are associated with the production of specialized soldiers. We asked whether colonies mitigate costs of production of specialized soldiers by simultaneously employing behavioral flexibility in nonspecialist workers that can augment defense capabilities at short time scales. We studied colonies of the stingless bee Tetragonisca angustula, a species that has 2 discrete nest-guarding tasks typically performed by majors: hovering guarding and standing guarding. Majors showed age polyethism across nest-guarding tasks, first hovering and then changing to the task of standing guarding after 1 week. Colonies were also able to reassign minors to guarding tasks when majors were experimentally removed. Replacement guards persisted in nest defense tasks until colonies produced enough majors to return to their initial state. Tetragonisca angustula colonies thus employed a coordinated set of specialization strategies in nest defense: morphologically specialized soldiers, age polyethism among soldiers within specific guarding tasks, and rapid flexible reallocation of nonspecialists to guarding during soldier loss. This mixed strategy achieves the benefits of a highly specialized defensive force while maintaining the potential for rapid reinforcement when soldiers are lost or colonies face unexpectedly intense attack.

Stingless bee floral visitation in the global tropics and subtropics

“…In the absence of an effective sting, they have evolved varied defence mechanisms including acid discharge (Roubik et al, 1987), suicidal biting (Shackleton et al, 2015) and sticking resin (Lehmberg et al, 2008). And they show a variety of social structures, whereby colonies may have multiple queens or single queens (Velthuis et al, 2006, Alves et al, 2011, workers may lay eggs regularly or be completely sterile (Sommeijer et al, 1999, Garcia Bulle Bueno et al, 2020, and the workers of some species include a "solider caste" (Baudier et al, 2019, Hammel et al, 2016, Grüter et al, 2012. All stingless bees, however, share a need to visit flowers for nectar for food, and almost all also collect pollen to provision their offspring (excluding a handful of Neotropical species that feed their offspring carrion or are cleptoparasites of other stingless bees; Sakagami et al, 1993, Mateus andNoll, 2004).…”

Soldier neural architecture is temporarily modality-specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula

“…Unlike ant soldiers, morphologically distinct soldiers of the stingless bee, Tetragonisca angustula [12] perform all of the tasks that non-soldier workers (henceforth "minors") perform but on an accelerated age-trajectory, switching to a repertoire dominated by colony defense tasks in the last two weeks of life (Figure 1) [13]. Soldiers of T. angustula further sub-specialize among different end-of-life defense tasks according to age [14]. Younger hovering guards primarily protect against heterospecific invasion using visual and volatile chemical cues while older standing guards on the nest entrance tube also intercept conspecific non-nestmates using close-range olfaction of non-volatile chemical cues [14][15][16][17][18].…”

“…Soldiers of T. angustula further sub-specialize among different end-of-life defense tasks according to age [14]. Younger hovering guards primarily protect against heterospecific invasion using visual and volatile chemical cues while older standing guards on the nest entrance tube also intercept conspecific non-nestmates using close-range olfaction of non-volatile chemical cues [14][15][16][17][18]. These tasks place different demands on visual and olfactory acuity and processing among these different soldier age groups.…”

“…Tetragonisca angustula soldiers work 34% to 41% more than non-soldier nestmates and have a lifetime task repertoire size that is 23% to 34% larger [13]. Soldiers of T. angustula also specialize and sub-specialize on defense tasks while minors do not typically perform colony defense [13] unless in a crisis [14]. By comparing brain volume and mushroom-body volume between soldiers and minors of T. angustula, we also tested whether the widely observed trends of smaller relative brain and mushroom-body size in eusocial insect soldiers is observed for stingless bee soldiers, despite soldiers in this species actually having a larger lifetime task repertoire.…”

Large body size variation is linked to low communication success in tandem running ants

“…because they are genetically more diverse, have been shown to collect food more successfully, respond better to environmental perturbations or produce more brood (Jones et al 2004; Mattila and Seeley 2007; Oldroyd and Fewell 2007; Modlmeier and Foitzik 2011). Workers of many species also differ in their morphology and this morphological variation is closely tied to division of labor in many species (ants: Hölldobler and Wilson 2009; bumblebees: Goulson et al 2002; stingless bees: Grüter et al 2017a, Baudier et al 2019; termites: Tian & Zhou 2014). Having different worker types for different tasks is likely to increase group performance because different worker types are more efficient at performing particular tasks (Oster and Wilson 1978; Powell and Franks 2005; Mertl and Traniello 2009; Grüter et al 2012, 2017b; Powell 2016).…”