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Young aphids avoid erroneous dropping when evading mammalian herbivores by combining input from two sensory modalities - PubMed

Young aphids avoid erroneous dropping when evading mammalian herbivores by combining input from two sensory modalities

Moshe Gish et al. PLoS One. 2012.

Abstract

Mammalian herbivores may incidentally ingest plant-dwelling insects while foraging. Adult pea aphids (Acyrthosiphon pisum) avoid this danger by dropping off their host plant after sensing the herbivore's warm and humid breath and the vibrations it causes while feeding. Aphid nymphs may also drop (to escape insect enemies), but because of their slow movement, have a lower chance of finding a new plant. We compared dropping rates of first-instar nymphs with those of adults, after exposing pea aphids to different combinations of simulated mammalian breath and vibrations. We hypothesized that nymphs would compensate for the greater risk they face on the ground by interpreting more conservatively the mammalian herbivore cues they perceive. Most adults dropped in response to breath alone, but nymphs rarely did so. Breath stimulus accompanied by one concurrent vibrational stimulus, caused a minor rise in adult dropping rates. Adding a second vibration during breath had no additional effect on adults. The nymphs, however, relied on a combination of the two types of stimuli, with a threefold increase in dropping rates when the breath was accompanied by one vibration, and a further doubling of dropping rates when the second vibration was added. The age-specificity of the aphids' herbivore detection mechanism is probably an adaptation to the different cost of dropping for the different age groups. Relying on a combination of stimuli from two sensory modalities enables the vulnerable nymphs to avoid costly mistakes. Our findings emphasize the importance of the direct trophic effect of mammalian herbivory for plant-dwelling insects.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Description of the leaf picking device.

A lever (A) is connected on one end to an upright post, so that it is free to rotate around the connection point (B). The distal end of the lever is connected to the post with a rubber band (C). The lever is lowered so that it is perpendicular to the post and the rubber band is taut. The lever is held in place with a moving stop (D). A small clothespin (F) is attached to a juvenile leaf at the base of a broad bean stem. A string is tied at one end to the clothespin (F), and at the other end attached to another clothespin (G) which is connected to the distal end of the lever. A slight pull on the string that is attached to the stop (E) releases the lever, allowing it to spring up and tear off the leaf. A second lever (H) is constructed in the same way. In the experiments that included two vibrations, first the lower lever (H) was released and then the upper lever (A). The device drawn here is in a “ready for operation" state at the beginning of an experiment.

Figure 2
Figure 2. Examination of pea aphid dropping response to different stimuli (and their combinations): details of experimental design.

The X axis denotes the time from the beginning of the experiment. In all treatments and controls N = 20.

Figure 3
Figure 3. Response of pea aphids (Acyrthosiphon pisum) to artificial breath and to vibration caused by a leaf picking device.

Error bars represent standard errors (±1 SE). In all treatments N = 20.

Figure 4
Figure 4. Increase in the dropping rates of pea aphid nymphs when exposed to a second vibration and its two controls.

Data are the average percentage of the nymphs in the colony that dropped (±1 SE). Percentage data were arcsine square-root transformed prior to analysis. X-axis labels denote: I: The difference between the response to a 2 s and a 4 s artificial breath. II: The difference between the response to one vibration and two consecutive vibrations. III: The difference between the response to one vibration during a 2 s artificial breath and two vibrations during a 4 s artificial breath. Each bar represents an average of the differences within 20 randomly assigned pairs of data from the two compared treatments.

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