Honey bees (genus Apis) are well known for the impressive suite of nest defenses they have evolved to protect their abundant stockpiles of food and the large colonies they sustain.
In Asia, honey bees have evolved under tremendous predatory pressure from social wasps in the genus Vespa, the most formidable of which are the giant hornets that attack colonies in groups, kill adult defenders, and prey on brood.
Heather R. Mattila, Gard W. Otis, Lien T. P. Nguyen, Hanh D. Pham, Olivia M. Knight, and Ngoc T. Phan document for the first time an extraordinary collective defense used by Apis cerana against the giant hornet Vespa soror.
In response to an attack by Vespa soror, Apis cerana workers foraged for and applied spots of animal feces around their nest entrances.
Fecal spotting increased after colonies were exposed either to naturally occurring attacks or to chemicals that scout hornets use to target colonies for mass attack.
Spotting continued for days after attacks ceased and occurred in response to V. soror, which frequently landed at and chewed on entrances to breach nests, but not Vespa velutina, a smaller hornet that rarely landed at entrances.
Moderate to heavy faecal spotting suppressed attempts by Vespa soror to penetrate nests by lowering the incidence of multiple-hornet attacks and substantially reducing the likelihood of them approaching and chewing on entrances.
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The authors argue that Apis cerana forages for animal feces because it has properties that repel this deadly predator from nest entrances, providing the first report of tool use by honey bees and the first evidence that they forage for solids that are not derived from plants.
Their study describes a remarkable weapon in the already sophisticated portfolio of defenses that honey bees have evolved in response to the predatory threats they face.
It also highlights the strong selective pressure honey bees will encounter if giant hornets, recently detected in western North America, become established.
In summary, we have documented fecal spotting as a novel defensive behavior that is used by Apis cerana honey bees to defend their nests against attack by the giant hornet Vespa soror, a poorly studied but formidable vespid that employs a mass-attack strategy similar to that used by its better-known sister species, Vespa mandarinia.
Viewed within the spectrum of counterstrategies that honey bees have evolved to defend their nests against a diverse array of threats, fecal spotting stands out as extraordinary for several reasons.
It marks the first report of hοney bees of any species foraging for materials that are not derived from plants or water-based fluids (excluding Apis florea colonies salvaging their own beeswax).
It is also the first clear-cut example of honey bees using a tool in nature (nests and the materials used to construct them are not generally considered tools, although some authors disagree).
Curious defensive behaviors within Apis tend to be innovatively threat specific. In that context, we show here that fecal spotting by Apis cerana is directed at V. soror hornets that attack in groups with the ruinous objective of occupying nests to prey on bee brood, but not at Vespa velutina hornets that prey on individual adult bees outside of nests only.
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However, much remains to be understood about this predator-prey interaction. What evolutionary steps underpinned the switch to foraging for filth (a new forage category) in the context of collecting tools for predator defense (a new function for foraging)?
What properties of feces provide A. cerana colonies with a measure of protection against V. soror attacks? How is spotting behaviour organized within A. cerana workforces?
Despite exerting enormous selective pressure on honey bees as one of their most deadly predators, remarkably little is understood about how V. soror or V. mandarinia workers recruit nestmates or coordinate their attacks.
Thus, basic aspects of the behavioral ecology of both predator and prey remain to be discovered before the role that feces plays in thwarting mass attacks by giant hornets can be fully appreciated.
These questions are more pressing with the recent introduction of giant Asian hornets to western North America.
The often negative consequences of the establishment of honey bee or hornet species into regions where predator-prey arms races have not had sufficient time to co-evolve highlight the importance for honey bees of having nest defenses that are tailored to meet the threats that different hornet species pose to their survival.