Visual contagion in prey defence signals can enhance honest defence

This blog post is provided by Shihao Dong, Ken Tan, and James C. Nieh and tells the #StoryBehindThePaper for their article “Visual contagion in prey defence signals can enhance honest defence, which was recently published in the Journal of Animal Ecology.

It’s a scene out of a horror film. In a sunny, peaceful glade, bees buzz out of their colony and return laden with nectar and pollen. A shadow appears, and a large, heavily armored hornet helicopters in front the colony, looking for easy victims. The Asian hornets, Vespa velutina and Vespa mandarinia (also known as the giant or yak-killing hornet) are infamous honey bee killers and invaders. In parts of the world, invading V. velutina have devastated European honey bees and there may be a growing threat from invasive giant hornets.

Yet evolution has tailored some very elegant solutions for the bee species that they prey upon and have co-evolved with. The Asian honey bee, Apis cerana, can attack the hornet by heat-balling it, forming a small swarm of stinging bees that encase the hornet, with an amazing defensive secret. They can cook it to death. As the defending bees furiously pump their muscles, they generate heat and carbon dioxide that helps, with the occasional armor-penetrating sting, to kill the hornet. This is also costly since the defending bees can overheat and die, and the hornet has its own defenses, powerful crushing mandibles and a potent stinger.

Defending to the death is, however, the normal strategy for a honey bee. If you have ever been stung, you will usually have noticed a stinger embedded in your skin while the bee flies off and dies because a vital part of its anatomy been ripped out. If you look closely, you may see the venom gland still active and pumping poison furiously into you, a painful deterrent that you will likely feel and remember for some time. But deterrence can take many forms.

In the arms race between bee and hornet, we expect a new strategy to evolve, warning signals. From a growling dog to the bright warning colors of a poison arrow frog, animals use these signals because the best alternative to combat is not fighting at all. There are thus a wide variety of signals that convey the message “back down, you’re not going to win this one.” In prey animals, a variant of this is the “pursuit-deterrence” signal, essentially “I’ve spotted you” and “pursuit is not going to work since I’m faster” or “I now have time to mount a great defense, give up”.

Apis cerana has such a signal, the “I See You” (ISY) signal, which warns the approaching hornet that it has been seen. Bees vibrate their wings and waggle their abdomens in a very specific way, and hornets can be deterred by this simple display. Why? A single ISY signal does not deter a hornet. Only a large number of synchronized and massed signals is effective because this conveys the honest ability of the colony to defend itself and form a heat ball.

Guard bee (lowest bee on right) performing the ISY signal in response to visually detecting a V. velutina hornet (not shown). (Photo taken by Dong Shihao)

My co-authors, Dong Shihao and Ken Tan, and I, decided to see what caused ISY signals. Using video playbacks (via an iPad), we were able to show that only playbacks of moving hornets (not a still hornet or a harmless local butterfly) would elicit ISY signals. But we wondered if the ISY signals might also draw in defenders even in the absence of a hornet. This worked and guards rushed towards a video playback of an ISY signaling bee.

Perhaps most interesting is that the ISY signal is also contagious! Guards not only were attracted, they started to immediately produce the ISY signal in response to the video of the signaling bee. Moreover, bees synchronized their signals, likely enhancing its overall effect against hornets.

Surprisingly, the scent of a hornet was not needed. Perhaps this is for the best because guards who are too far away to smell or hear the hornet can immediately head towards the threat. In some ways, it is like a fast chain reaction. But this poses a problem, the familiar issue of the boy crying wolf or, in modern parlance, “fake news.”

Multiple guard bees performing the ISY signal and successfully repulsing the hornet, which is seen flying away from the colony. (Photo taken by Dong Shihao)

There is often error in animal communication and a false ISY alarm could rapidly spread within the colony. This might not seem too bad, but a colony that is wasting its time rushing around to false predators is taking away time and resources better spent on other necessary tasks. Cue the opening scene of our busy foragers.

One solution to the problem of false information spread is that the bees are very selective about what they consider a true threat. The visual appearance and motion of the hornet alone could trigger ISY signals, but not a harmless butterfly. The second and most important safeguard against false reporting is that bees are even more choosy about what they consider to be a real ISY signal. We played back videos of bees performing ISY signals at different speeds, but only the correct bee image at the right speed caused other bees to respond.

However, there will always be some errors and we think that colonies are selected to reduce these mistakes to maximize their overall fitness. In addition, the bees seem most responsive to the playbacks during the hornet season, when hornets are actually present. In seasons when the hornets (which are also amazing social insects) are dormant, it is difficult to get any response from bees to the hornet videos. Perhaps this arises because it is fairly cold at those times of year and bee activity, including guarding, is reduced. However, an actual experience of hornets attacking at the right season may be needed to generate contagious ISY signals.

Can we learn from the bees about dealing with fake news? Individuals in a honey bee colony are completely interdependent. They cannot go out and make it on their own. Cooperation is paramount, especially when faced with large, heavily armored predators like hornets. A couple of hornets can kill thousands of bees in a single day. Yet through teamwork that correctly produces synchronized, massed ISY signals, they can get the hornet to back off without harming a single bee. Maybe there’s a lesson here….

Read the paper

Read the full paper: Dong, S, Tan, K, Nieh, JC. Visual contagion in prey defence signals can enhance honest defence. J Anim Ecol. 2020; 00: 1– 8.

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