Abstract

The prevalent way aphids accomplish colony defense against natural enemies is a mutualistic relationship with ants or the occurrence of a specialised soldier caste typcial for eusocial aphids, or even both. Despite a group-living life style of those aphid species lacking these defense lines, communal defense against natural predators has not yet been observed there. Individuals of Aphis nerii (Oleander aphid) and Uroleucon hypochoeridis, an aphid species feeding on Hypochoeris radicata (hairy cat's ear), show a behavioral response to visual stimulation in the form of spinning or twitching, which is often accompanied by coordinated kicks executed with hind legs. Interestingly, this behaviour is highly synchronized among members of a colony and repetitive visual stimulation caused strong habituation. Observations of natural aphid colonies revealed that a collective twitching and kicking response (CTKR) was frequently evoked during oviposition attempts of the parasitoid wasp Aphidius colemani and during attacks of aphidophagous larvae. CTKR effectively interrupted oviposition attempts of this parasitoid wasp and even repelled this parasitoid from colonies after evoking consecutive CTKRs. In contrast, solitary feeding A. nerii individuals were not able to successfully repel this parasitoid wasp. In addition, CTKR was also evoked through gentle substrate vibrations. Laser vibrometry of the substrate revealed twitching-associated vibrations that form a train of sharp acceleration peaks in the course of a CTKR. This suggests that visual signals in combination with twitching-related substrate vibrations may play an important role in synchronising defense among members of a colony. In both aphid species collective defense in encounters with different natural enemies was executed in a stereotypical way and was similar to CTKR evoked through visual stimulation. This cooperative defense behavior provides an example of a surprising sociality that can be found in some aphid species that are not expected to be social at all.

Highlights

  • Many aphid species constitute pests that inflict significant economic damage on cultivated and wild-growing plants

  • A detailed understanding of defense behavior executed by a pest and the behavior of natural enemies is of relevance for understanding both the general ecology and potential for biological pest control of aphid species

  • Twitching in both species was never accompanied by audible sound, sound production was described for other aphid species

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Summary

Introduction

Many aphid species constitute pests that inflict significant economic damage on cultivated and wild-growing plants Their damaging influence on hosts is mainly a consequence of a very rapid reproduction that quickly leads to large aphid colonies, which are often difficult to combat by means of biological pest control. In this context, a detailed understanding of defense behavior executed by a pest and the behavior of natural enemies is of relevance for understanding both the general ecology and potential for biological pest control of aphid species. Active defense against natural enemies at the colony level has not yet been described for group-living aphids lacking a soldier caste and a mutualistic relationship with ants

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