Outsourced hearing in an orb-weaving spider that uses its web as an auditory sensor.

SignificanceThe sense of hearing in all known animals relies on possessing auditory organs that are made up of cellular tissues and constrained by body sizes. We show that hearing in the orb-weaving spider is functionally outsourced to its extended phenotype, the proteinaceous self-manufactured web, and hence processes behavioral controllability. This finding opens new perspectives on animal extended cognition and hearing-the outsourcing and supersizing of auditory function in spiders. This study calls for reinvestigation of the remarkable evolutionary ecology and sensory ecology in spiders-one of the oldest land animals. The sensory modality of outsourced hearing provides a unique model for studying extended and regenerative sensing and presents new design features for inspiring novel acoustic flow detectors.

Manduca sexta caterpillars parasitized by the wasp Cotesia congregata stop chewing despite an intact motor system.

The parasitic wasp Cotesia congregata suppresses feeding in its host, the caterpillar Manduca sexta, during specific periods of wasp development. We examined both feeding behaviour and the neurophysiology of the mandibular closer muscle in parasitized and unparasitized control M. sexta to determine how the wasp may accomplish this. To test whether the wasps activated a pre-existing host mechanism for feeding cessation, we examined the microstructure of feeding behaviour in caterpillars that stopped feeding due to illness-induced anorexia or an impending moult. These microstructures were compared with that shown by parasitized caterpillars. While there were overall differences between parasitized and unparasitized caterpillars, the groups showed similar progression in feeding microstructure as feeding ended, suggesting a common pattern for terminating a meal. Parasitized caterpillars also consumed less leaf area in 100 bites than control caterpillars at around the same time their feeding microstructure changed. The decline in food consumption was accompanied by fewer spikes per burst and shorter burst durations in chewing muscle electromyograms. Similar extracellular results were obtained from the motorneuron of the mandibular closer muscle. However, chewing was dramatically re-activated in non-feeding parasitized caterpillars if the connectives posterior to the suboesophageal ganglion were severed. The same result was observed in unparasitized caterpillars given the same treatment. Our results suggest that the reduced feeding in parasitized caterpillars is not due to damage to the central pattern generator (CPG) for chewing, motor nerves or chewing muscles, but is more likely to be due to a suppression of chewing CPG activity by ascending or descending inputs.

Motor and mechanical bases of the courtship call of the male treehopper Umbonia crassicornis.

This study is a physiological, anatomical and biophysical analysis of how plant-borne vibrational signals are produced by the treehopper Umbonia crassicornis During courtship, males and females engage in a vibrational duet, with each producing a characteristic call. For males, this consists of a frequency-modulated tonal signal which is accompanied by rhythmic broad-band clicks. Although previous studies have described these complex signals in detail, little is known about how they are produced. By combining video recordings, electromyograms, dissections and mechanical modeling, we describe the mechanism by which the male produces his courtship signal. High-speed videos show that the tonal portion of the call is produced by periodic dorso-ventral movements of the abdomen, with a relatively large amplitude oscillation alternating with a smaller oscillation. Electromyograms from the muscles we identified that produce this motion reveal that they fire at half the frequency of the abdominal oscillation, throughout the frequency modulation of the tonal signal. Adding weight to the abdomen of a calling male reduces the frequency of motion, demonstrating that the abdominal motion is strongly influenced by its mechanical resonance. A mathematical model accounting for this resonance provides excellent qualitative agreement with measurements of both the muscle firing rate recorded electrophysiologically and the oscillatory motion of the abdomen as recorded in the high-speed video. The model, electromyograms and analysis of video recordings further suggest that the frequency modulation of the abdominal response is due to a simultaneous modulation in the muscle firing rate and a fluctuation in stiffness of the abdominal attachment.

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

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.

Behavioral and chemosensory responses to a host recognition cue by larvae of Pieris rapae.

Larvae of the cabbage white Pieris rapae are specialists on plants belonging to the family Brassicaceae (Cruciferae). Adult females have been shown to use the glucosinolate gluconasturtiin (phenylethylglucosinolate) as a recognition cue for cruciferous plants, so they can identify an appropriate host for oviposition (Huang and Renwick in J Chem Ecol 20:1025-1037, 1994). Here, we report our results from a study of the role of this glucosinolate in feeding preferences of P. rapae larvae. The larvae were allowed to choose between leaf disks from the non-host cowpea Vigna sinensis (Fabaceae) that were treated with pure gluconasturtiin in solvent, or solvent alone. Our results showed that gluconasturtiin is a feeding stimulant for P. rapae larvae. A series of chemosensory ablations revealed that this response is mediated by one set of taste sensilla, the sensilla styloconica. Electrophysiological tip recordings revealed two neurons in the lateral sensillum styloconicum that are sensitive to gluconasturtiin. These neurons show significantly higher firing frequencies with 4 mM gluconasturtiin added to the recording pipette than for recording solution alone. We propose that the sensitivity to gluconasturtiin shown by these two taste neurons is an important contributor to the animals' behavioral preference for this compound.

Chemosensory tuning to a host recognition cue in the facultative specialist larvae of the moth Manduca sexta.

Larvae of Manduca sexta are facultative specialists on plants in the family Solanaceae. Larvae reared on solanaceous foliage develop a strong preference for their host; otherwise, they remain polyphagous. The host-specific recognition cue in potato foliage for Manduca larvae is the steroidal glycoside, indioside D. Two pairs of galeal taste sensilla, the lateral and medial sensilla styloconica, are both necessary and sufficient for the feeding preferences of host-restricted larvae. We conducted electrophysiological tip recordings from sensilla of solanaceous or wheat germ diet-reared larvae. For each animal, recordings of the responses to indioside D, glucose, tomatine and KCl were compared. All responses included both phasic and tonic portions. The sensilla styloconica of solanaceous-reared larvae were tuned to indioside D, defined as maintaining a high sensitivity to indioside D, while showing lower sensitivity to other plant compounds. Half of the sensillar neurons of solanaceous-reared larvae were 'tuned' to indioside D, whereas those of wheat germ diet-reared larvae were not. The different responses between the two types of animals were a result of changes of individual receptor cells' responses in the sensilla. Feeding on solanaceous foliage therefore appears to result in a modification of the physiological responses of individual taste receptor cells that causes them to be tuned to the host-recognition cue indioside D. We propose that this tuning is the basis for the host-restricted larvae's strong behavioral preferences for solanaceous foliage.