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

Harvey, Jeffrey A.; Tanaka, Toshiharu; Kruidhof, Marjolein; Vet, Louise E. M.; Gols, Rieta

doi:10.1016/j.anbehav.2011.03.019

Cited by 20 publications

(32 citation statements)

References 44 publications

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“…After the wasps emerge, the caterpillar host becomes the cocoons' bodyguard (Kester and Jackson, 1996), as is seen in other parasitoid systems (e.g. Grosman et al, 2008;Harvey et al, 2011). (A parasitoid is an insect that develops by feeding off the body of another arthropod; Godfray, 1994.)…”

Section: Introductionmentioning

confidence: 99%

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

Adamo

Kovalko

Turnbull

et al. 2016

Journal of Experimental Biology

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Some parasites alter the behaviour of their hosts. The larvae of the parasitic wasp Cotesia congregata develop within the body of the caterpillar Manduca sexta. During the initial phase of wasp development, the host's behaviour remains unchanged. However, once the wasps begin to scrape their way out of the caterpillar, the caterpillar host stops feeding and moving spontaneously. We found that the caterpillar also temporarily lost sensation around the exit hole created by each emerging wasp. However, the caterpillars regained responsiveness to nociception in those areas within 1 day. The temporary reduction in skin sensitivity is probably important for wasp survival because it prevents the caterpillar from attacking the emerging wasp larvae with a defensive strike. We also found that expression of plasmatocyte spreading peptide (PSP) and spätzle genes increased in the fat body of the host during wasp emergence. This result supports the hypothesis that the exiting wasps induce a cytokine storm in their host. Injections of PSP suppressed feeding, suggesting that an augmented immune response may play a role in the suppression of host feeding. Injection of wasp larvae culture media into non-parasitized caterpillars reduced feeding, suggesting that substances secreted by the wasp larvae may help alter host behaviour.

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Section: Introductionmentioning

confidence: 99%

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

Adamo

Kovalko

Turnbull

et al. 2016

Journal of Experimental Biology

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“…pulchricornis against attack from the secondary hyperparasitoid G. agilis. In choice tests, susceptibility of the primary parasitoid cocoons to the hyperparasitoid was strongly correlated with retention or removal of the caterpillar after parasitoid egression and pupation (also see Harvey et al 2011). G. agilis signiÞcantly preferred to mount and oviposit in cocoons of Microplitis that were not attended by parasitized M. separata larvae.…”

Section: Discussionmentioning

confidence: 99%

“…The parasitoid cocoon is attached to the surface of a leaf, and the caudal appendages of the host caterpillar remain physically attached to the parasitoid cocoon. The parasitized caterpillar exhibits extremely aggressive behavior when it is disturbed, including frequent bouts of head thrashing, and biting (Harvey et al 2011). Still another solitary braconid wasp, Meteorus pulchricornis Wesmael (Hymenoptera: Braconidae), also emerges from an intact host which drops from the food plant and dies within a few hours.…”

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confidence: 99%

Differing Success of Defense Strategies in Two Parasitoid Wasps in Protecting their Pupae Against a Secondary Hyperparasitoid

Harvey

Gols

Tanaka

2011

Annals of the Entomological Society of America

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During their larval development, endoparasitoids are known to dispose of host resources in several different ways. Some parasitoid wasps consume most or all tissues of the host, whereas others consume a small fraction of host resources and either ensure that the host moves away from the pupation site or allow the host to remain close to the parasitoid cocoon(s). Using a single host species, Mythimna separata Walker (Lepidoptera: Noctuidae), this study compares the success of the two pupation strategies in the solitary parasitoids Microplitis sp. and Meteorus pulchricornis Wesmael (Hymenoptera: Braconidae) against attack from a secondary hyperparasitoid, Gelis agilis F. (Hymenoptera: Ichneumonidae). The caudal appendages of M. separata caterpillars parasitized by Microplitis sp. remain physically attached to parasitoid cocoons and the caterpillars behave aggressively when disturbed. However, after Me. pulchricornis larvae emerge from caterpillars of their host, M. separata, the parasitoid larvae pupate in cocoons that are suspended by a single thick thread that hangs 1–2 cm from under a leaf. In choice tests conducted in petri dishes, significantly fewer cocoons of Microplitis sp. attended by caterpillars than unattended cocoons were hyperparasitized by G. agilis. By contrast, Me. pulchricornis cocoons that were hanging from corn, Zea mays L., plants were hyperparasitized as frequently as those which were attached to leaves. We discuss the potentially different selection pressures generated among natural enemies such as predators and hyperparasitoids in determining optimal pupal defense strategies in primary parasitoids.

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“…The first example of this form of protection has been observed in three different Lepidoptera-Braconid wasp models: Pieris brassicae-Cotesia glomerata (Brodeur and Vet, 1994;Harvey et al, 2011), Manduca spp.-Cotesia congregata (Kester et al, 1996) and Thyrinteina leucocerae-Glyptapanteles sp. (Grosman et al, 2008) (Table1).…”

Section: Direct Protectionmentioning

confidence: 99%

“…Following egression of the parasitoid larvae from the host, the moribund caterpillar remains alive on the pupating parasitoids. Coiled on the cocoon masses, it exhibits violent head-thrashing movements, fending off predators (Kester and Jackson, 1996;Grosman et al, 2008) or hyperparasitoids (Harvey et al, 2011) (Fig.1A), essentially acting as a true bodyguard as this behaviour results in a reduction in mortality of the parasitic wasp pupae. In addition to displaying this aggressive defence behaviour, it has been shown that P. brassicae caterpillars also spin a silk web over the parasitoid cocoons (Fig.1B), reinforcing the physical barrier covering the parasitoid pupae (Brodeur and Vet, 1994).…”

Section: Direct Protectionmentioning

confidence: 99%

Diversity and evolution of bodyguard manipulation

Maure

Daoust

Brodeur

et al. 2013

Journal of Experimental Biology

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SummaryAmong the different strategies used by parasites to usurp the behaviour of their host, one of the most fascinating is bodyguard manipulation. While all classic examples of bodyguard manipulation involve insect parasitoids, induced protective behaviours have also evolved in other parasite-host systems, typically as specific dimensions of the total manipulation. For instance, parasites may manipulate the host to reduce host mortality during their development or to avoid predation by non-host predators. This type of host manipulation behaviour is rarely described, probably due to the fact that studies have mainly focused on predation enhancement rather than studying all the dimensions of the manipulation. Here, in addition to the classic cases of bodyguard manipulation, we also review these ʻbodyguard dimensionsʼ and propose extending the current definition of bodyguard manipulation to include the latter. We also discuss different evolutionary scenarios under which such manipulations could have evolved.

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

Cited by 20 publications

References 44 publications

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

Differing Success of Defense Strategies in Two Parasitoid Wasps in Protecting their Pupae Against a Secondary Hyperparasitoid

Diversity and evolution of bodyguard manipulation

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