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We studied the consequences of behavioural manipulation of the geometrid moth Thyrinteina leucocerae by its parasitoid wasp Glyptapanteles sp. Adult female parasitoids oviposit in first- and second-instar caterpillars of the moth, which feed on foliage of various trees of the Myrtaceae family, such as guava and eucalyptus.

Parasitized caterpillars continue developing and feeding until the 4 th or 5 th instar, when up to c. Grosman and A. Janssen, pers.


The larvae spin cocoons on a twig or leaf close to the caterpillar and pupate Fig. Subsequently, the host undergoes a series of behavioural changes, including cessation of feeding and moving. The most profound change in behaviour, however, is a strong increase of violent head-swings upon disturbance, in an apparent attempt to hit the agent of disturbance A. It has been suggested that such head-swings could serve as a defence of the parasitoid pupae against predation or hyperparasitism [20] , [22] , but evidence is lacking. We therefore quantified the effects of these behavioural changes on interactions with predators in the laboratory, as well as on survival of the parasitoid pupae in the field.

Full-grown larvae of the parasitoid egress from the caterpillar and spin cocoons close by their host. The host remains alive, stops feeding and moving, spins silk over the pupae, and responds to disturbance with violent head-swings supporting information.

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The caterpillar dies soon after the adult parasitoids emerge from the pupae. Photograph by Prof. Thyrinteina leucocerae and Glyptapanteles sp. The parasitoid species awaits further taxonomic description, and voucher specimens are deposited with Prof.

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Menezes Jr. The cups contained small 5—10 cm twigs of eucalyptus or guava with some 1—7 leaves, and were closed with a mesh.

The twigs were inserted into moist vermiculite to maintain leaf turgor. Fresh twigs were added twice per week. Moths were allowed to emerge and adults mated and oviposited inside the cages. Eggs were collected from the cages once a week, and were left to emerge in cages containing small trees. The host cultures were frequently supplemented with field-collected individuals. Recently emerged adult parasitoids, one female and 1—2 males, were incubated for 24 hours in a glass tube containing a piece of host plant leaf to allow them to mate.

Subsequently, the adult parasitoids were incubated for 24 hours in a plastic cup ml containing some leaves and up to 8 first-instar T. Parasitism is very rapid, occurring as a female parasitoid apparently walks over a host caterpillar. Immediate dissection of the caterpillar reveals up to 80 eggs inside A.

Parasitoid larvae egress from parasitized caterpillars through exit holes they make in the host cuticle and pupate after 11—16 days A. Grosman, pers. Parasitoid pupae were collected from the cups and incubated in glass tubes in the laboratory until adult emergence. As with the host, the parasitoid cultures were frequently supplemented with field-collected individuals. For all experiments, we used caterpillars emerging from the same egg batches, which were subdivided into groups: one group was exposed to parasitoids to obtain parasitized caterpillars, whereas the other group was not exposed i.

Because each group had an equal probability of containing hosts with aberrant behaviour, this minimized the possibility that any behavioural changes observed were due to parasitoids selecting hosts with atypical behaviour, rather than a consequence of parasitism [4].


First-instar hosts parasitized and unparasitized were placed individually on small E. Upon egression, half of the twigs with parasitoid pupae were cut off, while the caterpillar was left undisturbed on the plant. The twigs with pupae were stapled to a leaf close by an unparasitized caterpillar, resulting in four treatments: parasitized and unparasitized caterpillars either with or without parasitoid pupae close by. We marked the position of the caterpillars by tying a thin thread on the plant just behind the abdominal prolegs, taking care not to disturb the caterpillars.

Each subsequent day, we measured the distance moved by the caterpillar from the original thread by tying another thread just behind the abdominal prolegs. Caterpillar locomotion was scored until either five days after parasitoid egression or five days after the addition of parasitoid pupae. Caterpillar size was measured in a similar way with another piece of thread.

Locomotion of unparasitized caterpillars without pupae was scored until 5 days after the average caterpillar age at parasitoid egression 23 days. Although no parasitoid larvae egressed from unparasitized caterpillars, for brevity we refer to the movement of parasitized and unparasitized host before and after egression in all treatments. The distribution of movement data was non-normal due to zero inflation, even after transformations; we therefore used the more conservative non-parametric Kruskal-Wallis test [29] to compare locomotion among treatments before or after parasitoid egression.

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A Wilcoxon matched pairs test [29] was used to compare caterpillar locomotion before and after egression within treatments [29] using R statistical software R, version 2. Caterpillar body length was compared using a t-test.

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Predators of this genus attack parasitoid pupae as well as T. Subsequently, they were incubated for another day without parasitoid pupae to starve them, thus increasing their tendency to search for prey. Twigs with unparasitized or parasitized caterpillars with their pupae were inserted into a foam block, so that the twig was positioned vertically.

A starved predator was introduced gently at some 2—4 cm from the caterpillar without disturbing the latter, and was allowed to search. It was reintroduced if it left the twig before encountering the caterpillar or pupae. Parasitized and unparasitized caterpillars were tested in an alternate sequence, and each caterpillar and each predator was tested once.

Average observation time was 5. When the predator encountered the caterpillar, we scored the number of head-swings the caterpillar directed towards the predator, as well as the outcome of the interaction escape of the predator, predator knocked off by the head-swings. The number of head-swings by parasitized and unparasitized caterpillars were compared with a generalized linear model with quasi-Poisson error distribution to correct for overdispersion [30] , using R statistical software.

The numbers of predators that gave up or were chased away by the defending caterpillar were compared with a Fisher's exact test [29]. The vegetation covering the soil consisted mainly of grasses; the plantations were surrounded by more diverse native vegetation. One of the guava plantations was managed organically; the other plantation was not managed. We obtained parasitized caterpillars as described above.

All batches of parasitoid pupae that emerged on the same day were placed in the same field within one day of egression and pupation of the parasitoids. Each batch was attached to a separate guava tree by stapling the twig with or without caterpillar, depending on the treatment to a leaf, thus exposing it to predators and parasitoids.

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The number of pupae in batches with and without host did not differ significantly between treatments with host: A total of batches of parasitoid pupae were exposed in the two guava plantations. To measure mortality due to causes other than predation and hyperparasitism, we covered branches, to which twigs with pupae and caterpillars were attached, with a sleeve cage of fine mesh below referred to as unexposed batches.

Insect glue applied to the base of each branch prevented walking predators and parasitoids from accessing these unexposed batches. Batches were recollected after three days c. The proportion of pupae per batch which were eaten by predators or hyperparasitized was compared among treatments using GLM with quasi-binomial error distributions to correct for overdispersion [30] , using R statistical software. All caterpillars moved, and although parasitized caterpillars moved more than unparasitized caterpillars 7.

The two parasitized caterpillars that moved following parasitoid egression one with pupae and one without pupae covered a distance of 0. All parasitized caterpillars died soon after the adult parasitoids emerged from the pupae, some 6—7 days after egression of the larvae. This shows that the behavioural changes described here and below do not benefit the parasitized host. The distance covered by parasitized and unparasitized caterpillars was measured daily.

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Parasitoid pupae were either removed from parasitized caterpillars No pupae or not With pupae. Unparasitized caterpillars were supplied with pupae With pupae or not No pupae. Numbers of replicates are given in brackets. This indicates that the presence of parasitoid pupae does not induce a change in host behaviour.

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