The ‘usurpation hypothesis’ revisited: dying caterpillar repels attack from a hyperparasitoid wasp

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It has been posited that some parasitoid wasps ‘usurp’ their dying hosts as ‘bodyguards’ to protect the vulnerable parasitoid cocoons against attack from natural enemies such as predators or hyperparasitoids. Thus far, however, the hypothesis has been supported only in studies with insect predators. Two factors may account for this: first, hyperparasitoids, being more specialized than predators, are probably less easily rebuffed by the presence of an attending caterpillar; second, the host cocoon is used for reproduction by hyperparasitoids, but not by predators. We compared the survival of a solitary primary parasitoid, Microplitis sp., and successful parasitism by a secondary hyperparasitoid, Gelis agilis, from parasitoid cocoons with and without the presence of an ‘attending’ larva of the host, the armyworm, Mythimna separata. Mature Microplitis sp. larvae always emerge through the same host segment, leaving the posterior segments paralysed and attached to cocoons and the anterior segments freely moving. When disturbed by G. agilis females, M. separata larvae exhibited aggressive behaviour that repeatedly drove off approaching hyperparasitoids. In choice and no-choice experiments performed at 24 h intervals over 96 h, G. agilis successfully parasitized cocoons without attending caterpillars, but few cocoons with attending caterpillars were ever parasitized. Choice experiments, in which G. agilis wasps were released onto corn plants containing 24 h-old parasitoid cocoons with and without attending caterpillars, produced similar results. We provide the first experimental evidence that a solitary parasitoid usurps the behaviour of its host over several days as a ‘bodyguard’ against hyperparasitoids.