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Abstract
Social insect colonies constantly produce dead insects, which cause sanitary problems and potentially foster deadly pathogens and parasites. Hence, many social insects have evolved a variety of hygienic behaviors to remove cadavers from the colonies. To that end, they have to discriminate dead insects from live ones, where chemical cues should play important roles. In ants, bees and termites, such corpse recognition signals, also referred to as “death pheromones” or “necromones”, have been identified as fatty acids, specifically oleic acid and/or linoleic acid. Meanwhile, there has been no such report on social aphids. Here we attempted to identify the “death pheromone” of a gall-forming social aphid with second instar soldiers, Tuberaphis styraci, by making use of an artificial diet rearing system developed for this species. On the artificial diet plates, soldiers exhibited the typical cleaning behavior, pushing colony wastes with their heads continuously, against dead aphids but not against live aphids. GC-MS and GC-FID analyses revealed a remarkable increase of linoleic acid on the body surface of the dead aphids in comparison with the live aphids. When glass beads coated with either linoleic acid or body surface extract of the dead aphids were placed on the artificial diet plates, soldiers exhibited the cleaning behavior against the glass beads. A series of behavioral assays showed that (i) soldiers exhibit the cleaning behavior more frequently than non-soldiers, (ii) young soldiers perform the cleaning behavior more frequently than old soldiers, and (iii) the higher the concentration of linoleic acid is, the more active cleaning behavior is induced. Analysis of the lipids extracted from the aphids revealed that linoleic acid is mainly derived from phospholipids that constitute the cell membranes. In conclusion, we identified linoleic acid as the corpse recognition factor of the social aphid T. styraci. The commonality of the death pheromones across the divergent social insect groups (Hymenoptera, Blattodea and Hemiptera) highlights that these unsaturated fatty acids are generally produced by enzymatic autolysis of cell membranes after death and therefore amenable to utilization as a reliable signal of dead insects.
Highlights
In social insect colonies, a large number of individuals are living together within a limited nest space at a high population density, where dead insects are constantly produced
Considering that fatty acids are known to function as corpse recognition factors in other social insects such as ants, bees and termites [27,28,29,30,31,32,33,34], we extracted the body surface of live soldiers and non-soldiers as well as dead soldiers and non-soldiers with hexane, and analyzed the extracted fatty acid samples by gas chromatography-mass spectrometry (GC-MS) and gas chromatography with a flame ionization detector (GC-flame-ionization detector (FID))
This study presents the first report of death pheromone from social aphids
Summary
A large number of individuals are living together within a limited nest space at a high population density, where dead insects are constantly produced. Some aphids are social with specialized caste individuals called reproductives and soldiers [7,8,9]. These aphids parthenogenetically produce soldier nymphs that perform colony defense against natural enemies. Tuberaphis styraci is a social aphid that forms a large coral-shaped gall, up to 12 cm in diameter and hosting over 20,000 insects in maturity, on the tree Styrax obassia. While reproductive nymphs grow to adult and reproduce, soldiers neither grow nor reproduce but perform social tasks, namely colony defense against natural enemies and nest cleaning by disposing colony wastes [12, 19]. T. styraci provides a unique model for studies on the aphid sociality owing to the establishment of an artificial diet rearing system [20], by which the mechanisms underlying the density-dependent caste differentiation and regulation have been experimentally investigated in detail [21,22,23,24,25,26]
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