It's a scene straight out of a horror film - you look around and see dead bodies everywhere. They haven't just been killed either, they've been hollowed out from the inside-out leaving behind grotesque mummified shells. What would you do if you were confronted with such a macabre scene? Flee? Well, if you were an aphid, you'd probably just feel relieved and go about your business. Aphids, it seems, find security among the corpses of their peers.
Aphids, like almost all insects, are the targets of parasitic wasps that implant eggs inside their bodies. On hatching, the wasp grubs use the aphid as a living larder and eat their way out, leaving behind a mummified aphid-shaped husk.
These husks ought to be (quite literally) a dead give-away that parasites are afoot, valuable intel for any animal. But far from treating these bodies as a sign of danger, aphids actually see them as a reason to stick around. As Fievet says, "In human history, mummies had long been known to protect the dead; our study shows that in nature, mummies can also protect the living."
When food is scarce or danger abounds, aphids respond by producing winged offspring that can fly off to better, less threatening homes. They certainly react in this way when directly faced with parasitic wasps. Virgil Fievet from BIO3P wanted to see if they would do the same when surrounded by the mummified remains of their peers.
They placed individual grain aphids (Sitobion avenae) in cages, either alone or surrounded by mummies produced by the body-snatching wasp Aphidius rhopalosiphi. Unexpectedly, the aphids produced fewer winged offspring in the presence of the corpses, and the more corpses, the fewer fliers. Even if the mummies were placed on an adjacent plant, the aphids still behaved in the same way, investing in young that stayed put rather than left home.
It turns out that the aphids are not the only ones that glean information from the mummies. They're a message to the wasps too and apparently, they say "It's not worth it." When Fievet placed female wasps in a glass cage with aphid-infested plants, he found that they abandoned plants with 5 mummies and 10 healthy aphids more quickly than those with just 10 healthy aphids. While searching for their prey, the wasps bumped into fewer living aphids when the mummies were around, although whenever they found one, they were just as likely to attack it.
All in all, the aphids were actually safer among their deceased peers. In a group of 10 healthy individuals, an average of 75% were injected with eggs before the wasp flew away. If 5 mummies were present, just over half of the aphids were parasitized.
Fievet thinks that from the wasp's point of view, the dead aphids are a sign that this particular plant had already been mined for bodies. To avoid competition for other individuals, they soon flew off to find another group of aphids to attack. Perhaps, they were even trying to avoid the dangers of hyperparasites - wasps that attack other species of parasitic wasps.
The aphids meanwhile do a simple risk assessment and conclude that it's better to hide among the bodies of former peers than to find new, uncharted territory. Fievet has named this phenomenon the "dead zone effect" and he suggests that it may be found elsewhere in nature.
Wolves, for example, leave behind the carcasses of elk they have killed. Wolves are territorial hunters and to other elks, the presence of a fresh kill might indicate that the local hunters are temporarily satisfied. It might actually be better for them to stay close by than to move to an area where the local wolves may be hungrier. That will obviously need testing. For the moment, there is just one good example of the dead-zone effect but it's a strong one.
Reference: V. Fievet, P. Le Guigo, J. Casquet, D. Poinsot, Y. Outreman (2009). Living with the dead: when the body count rises, prey stick around Behavioral Ecology DOI: 10.1093/beheco/arp014
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Very cool research! And another brilliant summary.
It's nice to have some research to go along with an image like this one.
As a predator biologist (though primarily marine predators), I love stories like the wolf and the elk carcass. These are not mindless killing machines- they are far more devious than we give them credit for.
This is very interesting. I was at first confused as to why they didn't produce fliers, but it really does make since to stick around the dead. It's kind of like in movies, like in 28 Days Later where the main fellow hid amongst corpses while the military folk were trying to kill him. I've always though that if I were in a war and felt like I was about to be killed, the best thing to do would be to pretend I'm already dead. Is this something that become instinctual amongst aphids, or are they actually capable of this kind of logical induction?
Fantastic stuff. I would also wonder if it's not just that corpses indicate an area is "done", but if the search efficiency of the wasps is reduced in a minefield of corpses. So even if they wanted to find a juicy aphid, it would be harder to find. From the aphid's perspective, they get the benefits of sociality (reduced predation) without the cost (competition for resources).
Eric - what a pic! I was trying to find something to go with this article to no avail. But that's beautiful...
Dallas - I think it's fairly safe to say that they *aren't* capable of that level of logical induction.
Dan - I think a bit of both; it's probably that the wasp finds it harder to track down a live aphid and that it has less motivation to do so.
aren't aphid exuviia hollowed out shells? and if wasps see shells they know they're too late for egg laying and move to another plant.
Ed: Many thanks for your brilliant summary. You really did a great job! I found the metaphor of the horror film particularly attractive.
Dallas: Thank you, I was trying to find a movie scene to illustrate our results. I really have to improve my SF background. I agree with Ed, itâs safer to not consider aphids capable of logical induction. But who knows, they are so surprisingâ¦
Alex: Muratori had recently found that exuviae are recognised and attacked by wasps at the same level as aphids when both are present in the patch. Parasitoids wasted time in patch with exuviae but they are still motivated in searching for aphids. Muratori proposes however that aphids gain in protection by encounter-dilution effect when leaving their empty shells in the colony (http://www.biomedcentral.com/1471-2148/8/338/abstract/).
Parasitoids reacted to empty shells and mummies differently.
Virgil, thanks so much for coming here and taking questions from people. I wish more scientists would take this approach to public engagement - it really does help to foster interest in the area to be able to directly chat to the people doing the research. Bravo.
Cool. I saw this and was reminded of this paper on a similar issue:
Muratori FB, Damiens D, Hance T, Boivin G.
Bad housekeeping: why do aphids leave their exuviae inside the colony?
BMC Evol Biol. 2008 Dec 19; 8:338