Abstract
Aphids (Hemiptera: Aphididae) have a repertoire of defensive behaviors against insect predators and parasitoids that includes kicking, twitching, walking away and dropping off the plant. These defensive responses, which are most effective when aphids receive early warning of an approaching predator, are often initiated before the predator reaches the aphid. Although described before, the process of predator detection has practically never been experimentally investigated in aphids and it is currently unknown whether they can distinguish approaching predators from harmless insects, and which senses they use for pre-encounter predator detection. I therefore addressed these two questions by comparing seven behavioral responses of pea aphids (Acyrthosiphon pisum) to approaching predators (ladybugs) and non-predators (variegated caper bugs), to the plant-borne vibrations they generate and to visual cues. Aphids kicked, raised their bodies, withdrew their stylets and dropped more often in response to approaching ladybugs. Visual cues elicited only antennal movements. Body raising and antennal movements were more frequent in response to ladybug vibrations compared to caper bug vibrations. I found no evidence for predator-odor detection. Stylet withdrawal (preparation for escape) and dropping occurred in response to climbing insects but not to vibrations. I conclude that pea aphids use multimodal cues to detect approaching coccinellid predators. While visual cues alert the aphid without triggering defensive responses, vibrational cues are used to distinguish predators from non-predators. Future research on vibration patterns that aphids interpret as signs of danger may lead to the development of novel management techniques for one of the world’s worst crop pests.
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I would like to thank Moshe Inbar for invaluable advice and critical reading of the manuscript and Roni Amzaleg and Estee Antelis for technical assistance.
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Supplementary Informations
Supplementary video 1: A pea aphid pointing its antennae toward an approaching ladybug. Whenever an aphid detects danger, but sensory inputs are not sufficient for a decisive conclusion on a definite predator attack that merits immediate escape (contrast with Supplementary video 2), stretched antennae function as a tripwire, allowing the aphid to escape on time.
Supplementary file 1 (AVI 10188 kb)
Supplementary video 2: A pea aphid dropping from a plant after detecting an approaching ladybug from a distance. Notice that the aphid decides to drop before the ladybug reaches it.
Supplementary file 1 (AVI 3109 kb)
Supplementary video 3: A pea aphid raising its body and withdrawing its stylets from the plant in preparation for escape.
Supplementary file 1 (AVI 1518 kb)
Supplementary video 4: A pea aphid, seemingly indifferent to the presence of a non-predatory variegated caper bug.
Supplementary file 1 (AVI 2932 kb)
Supplementary video 5: A vibration transmission experiment in which plant-borne vibrations produced by a walking ladybug are transmitted to a second plant with a pea aphid on it (see Fig. 1). Notice the aphid's defensive responses- twitching and kicking.
Supplementary file 1 (AVI 7419 kb)
Supplementary video 6: A preliminary vibration transmission experiment (similar to the one in Supplementary video 5), conducted on a shaky laboratory bench. Notice that the aphids respond to ladybug induced vibrations despite clearly visible background noise.
Supplementary file 1 (AVI 10166 kb)
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Gish, M. Aphids detect approaching predators using plant-borne vibrations and visual cues. J Pest Sci 94, 1209–1219 (2021). https://doi.org/10.1007/s10340-020-01323-6
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DOI: https://doi.org/10.1007/s10340-020-01323-6