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Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains.

Gal R, Kaiser M, Haspel G, Libersat F - PLoS ONE (2014)

Bottom Line: Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose.This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets.We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and the Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

ABSTRACT
The parasitoid jewel wasp uses cockroaches as live food supply for its developing larva. To this end, the adult wasp stings a cockroach and injects venom directly inside its brain, turning the prey into a submissive 'zombie'. Here, we characterize the sensory arsenal on the wasp's stinger that enables the wasp to identify the brain target inside the cockroach's head. An electron microscopy study of the stinger reveals (a) cuticular depressions innervated by a single mechanosensory neuron, which are presumably campaniform sensilla; and (b) dome-shaped structures innervated by a single mechanosensory neuron and 4-5 chemosensory neurons, which are presumably contact-chemoreceptive sensilla. Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose. This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets. Accordingly, wasps demonstrate a normal stinging behavior when presented with cockroaches in which the brain was replaced with a hard (2.5%) agarose pellet. Conversely, wasps demonstrate a prolonged stinging behavior when the cockroach brain was either removed or replaced by a soft (0.5%) agarose pellet, or when stinger sensory organs were ablated prior to stinging. We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

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The stinger possesses mechanosensory and dual mechano-chemosensory organs.(A) Frontal view of the tip of the stinger (Scanning Electron Micrograph; SEM). DV: dorsal valve, VV1/2: first/second ventral valve. Dome-shaped sensilla (arrowheads) can be seen at the apex of the DV (two opposing triplets) and between serrations of the two VVs. (B) Cross-section of the stinger (light micrograph) showing the DV and two VVs enclosing the egg canal (EC). The tongue-and-groove structure of the rachis (Ra) and aulax (Au) enables intricate movements of the valves relative to each other. (C) Dorsal view of the stinger (SEM). The VVs in this image are extended distally to reveal their serrations (arrows) and a part of the EC. (D) Outlines of the stinger (distal part enlarged on the right) showing the distribution of different sensilla along the DV. Red arrows indicate the position of campaniform sensilla; black arrowheads indicate the position of dome-shaped sensilla. (E) External morphology of one campaniform sensillum (SEM). (F) A mechanosensory dendrite innervating a campaniform sensillum (Transmission Electron Micrograph; TEM). OvW: ovipositor wall, MT: microtubules, Sh: dendritic sheath. (G) External morphology of one dome-shaped sensillum (SEM). (H) A bundle of 4 chemosensory dendrites (CD) and 1 mechanosensory dendrite (MD) innervating a dome-shaped sensillum (TEM). OvW: ovipositor wall; Ap: apodeme. Sh: sheath. (I) Longitudinal section (TEM) through one dome-shaped sensillum demonstrating the apical pore (arrow) and sensillar sinus (SS). (J) Silver nitrate staining (light micrograph) of the stinger showing penetration of the tracer (black staining) through the pores of dome-shaped sensilla.
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pone-0089683-g002: The stinger possesses mechanosensory and dual mechano-chemosensory organs.(A) Frontal view of the tip of the stinger (Scanning Electron Micrograph; SEM). DV: dorsal valve, VV1/2: first/second ventral valve. Dome-shaped sensilla (arrowheads) can be seen at the apex of the DV (two opposing triplets) and between serrations of the two VVs. (B) Cross-section of the stinger (light micrograph) showing the DV and two VVs enclosing the egg canal (EC). The tongue-and-groove structure of the rachis (Ra) and aulax (Au) enables intricate movements of the valves relative to each other. (C) Dorsal view of the stinger (SEM). The VVs in this image are extended distally to reveal their serrations (arrows) and a part of the EC. (D) Outlines of the stinger (distal part enlarged on the right) showing the distribution of different sensilla along the DV. Red arrows indicate the position of campaniform sensilla; black arrowheads indicate the position of dome-shaped sensilla. (E) External morphology of one campaniform sensillum (SEM). (F) A mechanosensory dendrite innervating a campaniform sensillum (Transmission Electron Micrograph; TEM). OvW: ovipositor wall, MT: microtubules, Sh: dendritic sheath. (G) External morphology of one dome-shaped sensillum (SEM). (H) A bundle of 4 chemosensory dendrites (CD) and 1 mechanosensory dendrite (MD) innervating a dome-shaped sensillum (TEM). OvW: ovipositor wall; Ap: apodeme. Sh: sheath. (I) Longitudinal section (TEM) through one dome-shaped sensillum demonstrating the apical pore (arrow) and sensillar sinus (SS). (J) Silver nitrate staining (light micrograph) of the stinger showing penetration of the tracer (black staining) through the pores of dome-shaped sensilla.

Mentions: The jewel wasp’s stinger (Fig. 2) is approximately 2 mm in length, which is long enough to reach the cockroach’s brain when inserted from the neck [7]. As in many other parasitoids (e.g., [11], [14]), the stinger comprises three appendages (‘valves’) – an unpaired dorsal valve and a pair of ventral valves – which together enclose the egg canal and venom injection apparatus (Fig. 2A–C). A tongue-and-groove arrangement (the rachis and aulax; Fig. 2B) allows movement of the different valves relative to each other and enables intricate steering maneuvers [19]. Between 11 and 13 saw-teeth-like serrations reach 600–700 µm proximally from the apex on each of the ventral valves, whereas the dorsal valve is smooth and devoid of any serrations (Fig. 2A, C). Parasitoid wasps typically use such serrations to anchor the ovipositor inside the host’s integument during stinging, oviposition or transportation [13], [23]. The jewel wasp, however, is an ectoparasitoid and its stinger only penetrates through the cockroach’s integument during the stinging process. Hence, it is reasonable to assume that these serrations anchor the ventral valves inside the cockroach’s head capsule as the distal part of the dorsal valve penetrates through the ganglionic sheath and into the cockroach’s brain. The dorsal valve thus appears to play a more active role in the brain-recognition process.


Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains.

Gal R, Kaiser M, Haspel G, Libersat F - PLoS ONE (2014)

The stinger possesses mechanosensory and dual mechano-chemosensory organs.(A) Frontal view of the tip of the stinger (Scanning Electron Micrograph; SEM). DV: dorsal valve, VV1/2: first/second ventral valve. Dome-shaped sensilla (arrowheads) can be seen at the apex of the DV (two opposing triplets) and between serrations of the two VVs. (B) Cross-section of the stinger (light micrograph) showing the DV and two VVs enclosing the egg canal (EC). The tongue-and-groove structure of the rachis (Ra) and aulax (Au) enables intricate movements of the valves relative to each other. (C) Dorsal view of the stinger (SEM). The VVs in this image are extended distally to reveal their serrations (arrows) and a part of the EC. (D) Outlines of the stinger (distal part enlarged on the right) showing the distribution of different sensilla along the DV. Red arrows indicate the position of campaniform sensilla; black arrowheads indicate the position of dome-shaped sensilla. (E) External morphology of one campaniform sensillum (SEM). (F) A mechanosensory dendrite innervating a campaniform sensillum (Transmission Electron Micrograph; TEM). OvW: ovipositor wall, MT: microtubules, Sh: dendritic sheath. (G) External morphology of one dome-shaped sensillum (SEM). (H) A bundle of 4 chemosensory dendrites (CD) and 1 mechanosensory dendrite (MD) innervating a dome-shaped sensillum (TEM). OvW: ovipositor wall; Ap: apodeme. Sh: sheath. (I) Longitudinal section (TEM) through one dome-shaped sensillum demonstrating the apical pore (arrow) and sensillar sinus (SS). (J) Silver nitrate staining (light micrograph) of the stinger showing penetration of the tracer (black staining) through the pores of dome-shaped sensilla.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3935893&req=5

pone-0089683-g002: The stinger possesses mechanosensory and dual mechano-chemosensory organs.(A) Frontal view of the tip of the stinger (Scanning Electron Micrograph; SEM). DV: dorsal valve, VV1/2: first/second ventral valve. Dome-shaped sensilla (arrowheads) can be seen at the apex of the DV (two opposing triplets) and between serrations of the two VVs. (B) Cross-section of the stinger (light micrograph) showing the DV and two VVs enclosing the egg canal (EC). The tongue-and-groove structure of the rachis (Ra) and aulax (Au) enables intricate movements of the valves relative to each other. (C) Dorsal view of the stinger (SEM). The VVs in this image are extended distally to reveal their serrations (arrows) and a part of the EC. (D) Outlines of the stinger (distal part enlarged on the right) showing the distribution of different sensilla along the DV. Red arrows indicate the position of campaniform sensilla; black arrowheads indicate the position of dome-shaped sensilla. (E) External morphology of one campaniform sensillum (SEM). (F) A mechanosensory dendrite innervating a campaniform sensillum (Transmission Electron Micrograph; TEM). OvW: ovipositor wall, MT: microtubules, Sh: dendritic sheath. (G) External morphology of one dome-shaped sensillum (SEM). (H) A bundle of 4 chemosensory dendrites (CD) and 1 mechanosensory dendrite (MD) innervating a dome-shaped sensillum (TEM). OvW: ovipositor wall; Ap: apodeme. Sh: sheath. (I) Longitudinal section (TEM) through one dome-shaped sensillum demonstrating the apical pore (arrow) and sensillar sinus (SS). (J) Silver nitrate staining (light micrograph) of the stinger showing penetration of the tracer (black staining) through the pores of dome-shaped sensilla.
Mentions: The jewel wasp’s stinger (Fig. 2) is approximately 2 mm in length, which is long enough to reach the cockroach’s brain when inserted from the neck [7]. As in many other parasitoids (e.g., [11], [14]), the stinger comprises three appendages (‘valves’) – an unpaired dorsal valve and a pair of ventral valves – which together enclose the egg canal and venom injection apparatus (Fig. 2A–C). A tongue-and-groove arrangement (the rachis and aulax; Fig. 2B) allows movement of the different valves relative to each other and enables intricate steering maneuvers [19]. Between 11 and 13 saw-teeth-like serrations reach 600–700 µm proximally from the apex on each of the ventral valves, whereas the dorsal valve is smooth and devoid of any serrations (Fig. 2A, C). Parasitoid wasps typically use such serrations to anchor the ovipositor inside the host’s integument during stinging, oviposition or transportation [13], [23]. The jewel wasp, however, is an ectoparasitoid and its stinger only penetrates through the cockroach’s integument during the stinging process. Hence, it is reasonable to assume that these serrations anchor the ventral valves inside the cockroach’s head capsule as the distal part of the dorsal valve penetrates through the ganglionic sheath and into the cockroach’s brain. The dorsal valve thus appears to play a more active role in the brain-recognition process.

Bottom Line: Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose.This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets.We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and the Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

ABSTRACT
The parasitoid jewel wasp uses cockroaches as live food supply for its developing larva. To this end, the adult wasp stings a cockroach and injects venom directly inside its brain, turning the prey into a submissive 'zombie'. Here, we characterize the sensory arsenal on the wasp's stinger that enables the wasp to identify the brain target inside the cockroach's head. An electron microscopy study of the stinger reveals (a) cuticular depressions innervated by a single mechanosensory neuron, which are presumably campaniform sensilla; and (b) dome-shaped structures innervated by a single mechanosensory neuron and 4-5 chemosensory neurons, which are presumably contact-chemoreceptive sensilla. Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose. This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets. Accordingly, wasps demonstrate a normal stinging behavior when presented with cockroaches in which the brain was replaced with a hard (2.5%) agarose pellet. Conversely, wasps demonstrate a prolonged stinging behavior when the cockroach brain was either removed or replaced by a soft (0.5%) agarose pellet, or when stinger sensory organs were ablated prior to stinging. We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

Show MeSH
Related in: MedlinePlus