Young Aphids Avoid Erroneous Dropping when Evading Mammalian Herbivores by Combining Input from Two Sensory Modalities

Moshe Gish,Amots Dafni,Moshe Inbar,Martin Heil

doi:10.1371/journal.pone.0032706

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.

Highlights

Juvenile animals are usually smaller and less agile than adults
Experimental plants and animals Pea aphids were reared on broad bean plants, Vicia faba L., that were planted in plastic cups filled with a commercial growing medium and kept in the laboratory at 22uC61uC, 65%610% relative humidity (RH) and a photoperiod of 16:8 L:D
We found that pea aphid nymphs have a different tipping point from adults when dropping in response to cues that are typical of mammalian herbivore feeding; most of the adults escape incidental ingestion upon sensing the herbivore’s breath alone, while nymphs tend to drop only when sensing concurrent breath and vibrational stimuli (Fig. 3)

Summary

Introduction

Juvenile animals are usually smaller and less agile than adults. As a consequence, young are often more vulnerable to attack by predators. Some predators take advantage of this and prefer to attack juveniles [1,2] This difference between juveniles and adults has led in many cases to the development of agespecific, passive and active defense strategies. On the other hand, the adults are the cryptic ones and the juveniles wave their brightly colored tails to deflect predators away from their body [5]. Another way of defending against predators is to display aggression. Adult American lobsters threaten and attack an approaching predator as opposed to the juveniles which prefer to retreat [6,7]. Juveniles may compensate for their higher vulnerability to predators by escaping, more frequently than adults, to a different part of their habitat where they are camouflaged or less accessible, as demonstrated in grasshoppers [11] and freshwater snails [12]

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