Calling Leon Kennedy

Players of Resident Evil 4 who explored every corner of the sewer filled with hideous insects may remember reading the research Luis left behind describing creatures that changed their behavior due to the presence of parasites. The report about creatures such as Dicrocoelium dendriticum is actually fairly accurate, given its brevity, but doesn't address some important questions. For instance, most of the research on behavioral modifications of this kind comes from laboratory research that may not reflect what actually happens in nature. However, with field research it is sometimes difficult to distinguish aberrant behavior arising due to parasitism from preferential parasitism of aberrantly-behaving hosts. In a recent article in the online open-access journal PLoS ONE, a team of researchers from the University of Amsterdam and Federal University of Viçosa in Brazil set out to get a better grasp on behavioral changes in a caterpillar following parasitism by a wasp.

The wasp in this case is actually a parasitoid species, which differs from a classical parasite in that the death of the host is a certainty. The authors bred both the wasps and the host caterpillars in captivity, and randomly chose the caterpillars that would be hosts. This ensured that observed differences in behavior would be solely the result of parasitism and not some preference on the part of the wasps. Implantation of the eggs was apparently rapid and painless: just by walking over the caterpillars the wasps were able to lay as many as 80 eggs at a go. Perhaps this observation fills you with horror, in which case I say: you are not alone.

After this, the caterpillars were taken out of the lab and allowed to mature on trees on campus at Viçosa. Their movement and behavior were monitored out in the wild and also under controlled conditions in the laboratory. During the incubation of the larvae inside the caterpillar, no significant differences in behavior were observed. Hosts moved and ate at essentially the same rates as their unparasitized brethren. Once the wasp larvae emerged and pupated, however, the hosts' behavior changed dramatically. They ceased to move along tree branches or eat, and instead hovered over the pupae (check out Figure 1 and the supplemental movie 1), swinging their heads at potential predators.

The hypothesis that the parasitoids control host behavior to gain some sort of advantage would suggest a couple of predictions. One is that the behavioral changes are exclusively associated with parasitized caterpillars. Another is that the behavioral changes increase the probability that the parasitoids survive to adulthood. In addition, one might expect that the behavior has no benefit for the host. All of these predictions turn out to be accurate.

Unparasitized caterpillars from the same batches of eggs as the hosts did not show any of the host behaviors, strongly supporting the contention that the behavioral difference is solely the result of the parasitoids. In addition, when unparasitized caterpillars were placed on branches with pupae, they ignored both the pupae themselves and potential predators. The modification clearly has benefits for the wasps, as Janssen et al. found that the presence of a zombie caterpillar doubles the survival chances of the pupae. As for the caterpillar hosts, they die around the time that the adult wasps emerge, without themselves reaching maturity. That means that there's a great deal of benefit for the wasps, and none for the poor caterpillars.

What actually causes the change in behavior? Because it persists even after the pupae themselves have been removed from the vicinity, because the pupae alone do not induce behavioral changes in unparasitized caterpillars, and because the time between parasitism and larval emergence is about a fortnight, the authors conclude that neither the pupae or adult wasps are directly responsible. Dissection of the hosts after egression indicated that one or two active larvae were usually left behind. Similar to the case of D. dendriticum, these lingering parasitoids may be sacrificed to protect their brethren by manipulating their host.

There's no need to go grab your shotgun: these wasps are pretty small and aren't about to go parasitizing humans. In addition, the behavioral effect, though striking, seems to involve very general manipulations. Las Plagas these ain't. Still the mindlessly aggressive protection of the pupae calls to mind a boss monster, helplessly guarding the hideous young of an alien species. Best keep Leon on speed dial, just in case.

Carl Zimmer has also covered this over at The Loom. He's a great writer, so check it out... and also consider grabbing a copy of his new book Microcosm. Ed Yong has his own excellent article on this research.

1. Grosman, A.H., Janssen, A., de Brito, E.F., Cordeiro, E.G., Colares, F., Fonseca, J.O., Lima, E.R., Pallini, A., Sabelis, M.W., Raine, N.E. (2008). Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators. PLoS ONE, 3(6), e2276. DOI: 10.1371/journal.pone.0002276 OPEN ACCESS