Wasps use fumigation to keep food fresh

Some animals feed their young with breast milk. Some rely on their offspring fending for themselves. But others, like the wasp species Philanthus, also known as the European beewolf or bee-killer wasp, have a more gruesome strategy: they paralyse a bee, drag it to their lair and lay an egg on it. When it hatches, the wasp larva eats the corpse. We knew already that the wasps use several tactics to keep the food fresh, including bug-suppressing lipids and doses of friendly microbes, but now, as he explains to Chris Smith, Erhard Strohm has discovered they also use an even more ingenious strategy: fumigation…

Erhard - Insect eggs, actually the eggs of the European beewolf, fight off fungi using a gas. They have to do it because beewolves hunt honeybees and provide paralysed honeybees for their progeny as food. They bring these paralysed honeybees into underground nests, where there's a humid and warm microclimate. Because of this the bees will quickly be overgrown by fungi. And beewolves have already evolved two different mechanisms that we have reported on earlier: the bees are embalmed with hydrocarbons like lipids so that fungi grow less rapidly; the other thing is that beewolves have a symbiosis with bacteria, and these bacteria are cultivated into antennae and the females deliver these anterior to the larvae, and they integrate these bacteria into the cocoon where the bacteria produce antibiotics. But these two mechanisms were not enough to result in such a high survival of the larvae - so there must be a third mechanism. Actually it was the observation that when we open the observation cages we were reminded of chlorine of swimming pools. So we started to ask where this smell comes from, and it turned out that it was emanated from the eggs actually.

Chris - So you smell something reminiscent of swimming pools coming from these bees which have been embalmed by the wasp as future food for its larvae to eat. So where's that smell coming from then? The actual bee that's been embalmed?

Erhard - It's coming from the egg. You can just remove the egg from the bee and you find that the egg is smelling actually.

Chris - So the egg is releasing something, you could smell something coming from the egg reminiscent of a swimming pool: chlorine, but not necessarily chlorine. And it's that you thought that could be protecting the corpse of the bee?

Erhard - Yes. And we went on to identify this gas. We found that it was nitric oxide, and this nitric oxide is easily oxidised to nitrogen dioxide, and this nitrogen dioxide is what smells like chlorine.

Chris - And what does it do to microbes, that nitrogen dioxide? Does it kill them off?

Erhard - Well both nitric oxide and nitrogen dioxide are both radicals, and they will react with biomolecules and they will kill the fungi.

Chris - Why don't they kill the wasp larva then inside the egg? And also why don't they wipe out the good microbiota that the female wasp has wiped off of her antennae and impregnated onto the corpse of the bee?

Erhard - Yes, this is one of the most puzzling things about this whole story. We don't actually know how the egg is protected. We think the embryo in the egg produces this NO, and this NO might be transported to the eggshell with special transport molecules, and then it's delivered outside, but it can't go back into the egg. So maybe it's just a layer outside or on the outside of the egg that prevents these nitrogen oxides coming back into the egg. And the other question, why the bacteria that are delivered by the beewolf female into the blood cell are not affected, also is not known yet. We can speculate that these bacteria have evolved a resistance against these nitrogen oxides but we don't know yet.

Chris - Given the advantage to the fungus is so huge, that there's all this wonderful bee food to eat if you're not being poisoned by nitric oxide, why hasn't the fungus evolved to be more resilient in the same way that you're presuming that the microbiota which are being added to the bee by the female wasp, and the larva growing inside the egg; why has the fungus not developed its own resistance?

Erhard - Well if there would be selection for resistance in the fungus, they certainly would have evolved a mechanism to withstand the nitric oxide or nitrogen dioxide, but there isn't huge selection on the side of the fungus because in all brood cells there would be different fungi. And because of this non specialisation there is no selection. The symbiotic bacteria are always exposed to the nitrogen oxides, so there will be strong selection on them to produce resistance. The same with the embryo of course.

Chris - And do the larvae shut down this overproduction of NO as their gestation develops?

Erhard - Well a very interesting aspect is that the gas is only produced during a short period of about two hours and it starts about 14 hours after egg laying, and the gas will be produced for two hours and then it fades away. So it seems that there is one time point of huge concentration of this gas, and during this time the fungi will be killed and then the gas will disappear from the brood cell, so the larvae then they hatch will not be affected anymore by the gas.