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Alteration of host behaviour
What can parasitoid wasps teach us about decision-making in insects?
Frederic Libersat, Ram Gal
Journal of Experimental Biology 2013 216: 47-55; doi: 10.1242/jeb.073999
Frederic Libersat
Department of Life Sciences, Ben-Gurion University of the Negev, PO Box 653, Be’er Sheva, 84105 Israel
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  • For correspondence: libersat@bgu.ac.il
Ram Gal
Department of Life Sciences, Ben-Gurion University of the Negev, PO Box 653, Be’er Sheva, 84105 Israel
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    Fig. 1.

    Life cycle of the parasitoid jewel wasp Ampulex compressa. An adult wasp stings a cockroach into the head (A) to manipulate the cockroach behaviour. The wasp then cuts the cockroach’s antennae (B) to drink hemolymph, and then leads the stung cockroach into a nest to lay an egg on its cuticle. The hatching larva (C) feeds on the cockroach, pupates inside its abdomen and emerges roughly 30 days later (D).

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    Fig. 2.

    The wasp stings directly inside the cockroach’s cerebral ganglia. (A) Autoradiographs of the supra-esophageal ganglion (SupEG) and sub-esophageal ganglion (SEG) of a cockroach stung by a radio-labelled wasp. Black staining indicates the presence of venom. Adapted from Haspel et al. (Haspel et al., 2003). (B) Suggested mechanism of the stinging process. The wasp’s stinger (St; scanning electron micrograph of the stinger, scaled to the schematic drawing of the cockroach’s head) penetrates through the neck to reach both cerebral ganglia. Es, esophagus.

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    Fig. 3.

    The wasp’s venom selectively affects walking. (A) Electromyographic (EMG) recording from the metathoracic coxa of a cockroach before (top) and after (bottom) a wasp’s sting. Before the sting, a wind stimulus applied to the cerci (vertical arrows) evokes rhythmic slow (Ds) and fast (Df) coxal depressor activity. After a sting, in contrast, the same stimulus evokes only tonic Ds firing, which is not accompanied by Df potentials. (B) EMG recordings from the metathoracic leg coxa during righting behavior in a control (top) and a stung (bottom) cockroach. Both Ds and Df potentials can be observed. (C) Simultaneous EMG recordings from the coxae of three legs (R2, right mesothoracic; L3/R3, left/right metathoracic) during swimming in a stung cockroach. The alternating tripod gait can be distinguished. (D) Simultaneous EMG recordings from three wings (R1, right forewing; R2/L2, right/left hindwings) demonstrating normal flying motor pattern in a stung cockroach. (B–D) Adapted from Gal and Libersat (Gal and Libersat, 2008).

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    Fig. 4.

    Stung cockroaches show elevated behavioural thresholds for walking. (A) Cockroaches were subjected to escapable foot shocks in a modified shuttle box before (time 0) and at different time points after the sting (or after handling, in controls). The threshold voltage required to elicit escape responses gradually and reversibly increases in stung but not in control individuals. Data points labelled with the same letter are not significantly different. (B) Stung cockroaches were positioned in a walking posture on a slippery surface to allow tethered walking, recorded with a photoresistor placed beneath the mesothoracic leg. Motion traces of the mesothoracic leg show the response to trains of brief (arrowheads) tactile stimuli in the same cockroach before and 180 min after a sting. A single stimulus evokes walking before (top) but not after (middle) the sting. However, four consecutive stimuli applied to the stung cockroach (bottom) evoke a walking episode that outlasts the stimuli train. Walking evoked by this supra-threshold stimulus is significantly slower in the stung cockroach (note the different time scales in the top and bottom panels). Adapted from Gal and Libersat (Gal and Libersat, 2008).

  • Fig. 5.
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    Fig. 5.

    Swimming motion tracks during a 1-min trial in a modified forced swimming test. A control cockroach (left) continuously swims to escape the water-filled arena, demonstrating a period of immobility (thick line) only towards the end of the trial (asterisk). In contrast, a stung cockroach initiates swimming similar to that of the control but ‘despairs’ faster, spending most of the trial passively floating on the water surface. Adapted from Gal and Libersat (Gal and Libersat, 2008).

  • Fig. 6.
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    Fig. 6.

    Spontaneous (A) and evoked (B) neuronal activity in the sub-esophageal ganglion (SEG) is inhibited in stung cockroaches. Neuronal activity was recorded with an extracellular bipolar stereode from the middle of the SEG. The dashed area in the top traces in A is expanded in the bottom traces. Arrowheads in B represent the onset of a wind stimulus applied to the cerci. Adapted from Gal and Libersat (Gal and Libersat, 2008).

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Keywords

  • Ampulex compressa
  • Behaviour
  • neuron
  • Motivation
  • Periplaneta americana
  • venom

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Alteration of host behaviour
What can parasitoid wasps teach us about decision-making in insects?
Frederic Libersat, Ram Gal
Journal of Experimental Biology 2013 216: 47-55; doi: 10.1242/jeb.073999
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Alteration of host behaviour
What can parasitoid wasps teach us about decision-making in insects?
Frederic Libersat, Ram Gal
Journal of Experimental Biology 2013 216: 47-55; doi: 10.1242/jeb.073999

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Article navigation

  • Top
  • Article
    • Summary
    • Introduction: manipulation of host behaviour in parasitoid wasps
    • The parasitoid jewel wasp: a case study
    • The jewel wasp injects venom directly inside the cockroach’s CNS
    • Central aspects of the venom-induced hypokinesia
    • Involvement of the SEG in the venom-induced hypokinesia
    • Possible role of the SupEG in the venom-induced hypokinesia
    • Does the venom affect bioaminergic neurons to induce hypokinesia?
    • Concluding remarks
    • Future prospects: cellular and molecular mechanisms of the venom-induced behavioural manipulation
    • FOOTNOTES
    • References
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