Dropping aphids and their alarm pheromones

Fortunately for the organic gardener, aphids have many predators: hoverfly larvae, lacewings, ladybirds, shield bugs and spiders eat them in numbers. Although aphids appear defenceless against their predators, they have evolved a suite of antipredator responses. Some aphids have warning coloration and sequester chemicals from their feeding plants that are distasteful or toxic to their predators, other release toxic chemicals or waxes and a few have a hard-skinned soldier caste to defend the colony, yet others maintain an army of ants that defend them. The most common form of defence - both against predators or parasitoids - is however, behavioural: the aphids move away or drop from the leaf they are feeding on when they sense an approaching predator.
 Dropping is very effective in reducing immediate risk: aphids fall away from the approaching danger onto the ground. Once there other costs become apparent: the aphid may be far from the host plant and is exposed to ground predators or to desiccation.
 The orange tree in my conservatory is infested with aphids. I took advantage of the abundance of 7 spot ladybirds in the garden and brought a few onto the tree, placing them on particularly infested branches. I was pleasantly surprised by the eagerness with which the ladybirds took to the intended job. They started munching aphids straight away, clearing whole shoots in a few minutes. After a little observation, however, it became apparent that it was the aphid's behaviour which was mostly responsible for the shoots being cleared. The undisturbed aphids sat motionless, on a living carpet feeding on the tender leaf sap nearby. In contrast, as soon as a ladybird attacked, the aphids on the same leaf came alive and some started to move away, going into another leaf, while many aphids dropped to the ground as the ladybird fed on their unfortunate siblings. The following two photos illustrate this. They were taken about 27 seconds apart. In the first one, notice the three aphids on the tip of the leaf. In the second photo, these aphids have dropped to the ground, leaving just a couple of aphid molts stuck to the leaf tip, while the ladybird is still feeding on an aphid, motionless.

 Ladybirds are very effective at eliciting the drop response from aphids, especially when compared to smaller, less energetic feeders, as demonstrated in experiments by John Losey and Robert Denno on pea aphids feeding on alfalfa exposed to a predator insect.

This means that on average 60% of aphids feeding on a plant stem dropped to the ground when a 7 spot ladybird (Coccinella septempunctata) was introduced, in sharp contrast to the lower dropping response to the bugs and the control. Given the higher mortality of aphids on the ground, it follows that ladybirds would be very effective clearing aphid infestations through direct predation, and their indirect effect on aphids dropping from the plant.
 What mechanisms are responsible for this dropping behaviour? or, put differently, how do aphids sense that a predator is approaching? Dropping behaviour happens in response to predator contact, vibrations generated by the predator, or in response to an alarm pheromone secreted by individual aphids when attacked. This chemical signal, (E)-ß-farnesene (EBF), is secreted in dropplets by the cornicles, little tubes at the rear of the aphid, and they may impregnate the predator, which in its next move will elicit the dropping response before actually attacking another aphid.
 The release of an alarm pheromone by an individual that is likely to be eaten by a predator seems paradoxical. What benefit can this individual gain from its production? An alarm pheromone can be adaptive when the benefit is shared by relatives. This is indeed the case in aphids: groups of aphids feeding in close contact are likely to be members of the same clone, that is, they are genetically identical, as aphids often reproduce parthenogenetically. The alarm pheromone also has longer lasting effects benefiting the individual relatives, as the aphids that have been exposed to the chemical tend to produce winged offspring, which will likely disperse away from predators, in the case of the ladybird attacker, they will be likely to avoid the following generation of ladybird larvae.

References
LOSEY, J., & DENNO, R. (1998). The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology, 23 (1), 53-61 DOI: 10.1046/j.1365-2311.1998.00102.x
Schwartzberg, E., Kunert, G., Stephan, C., David, A., Röse, U., Gershenzon, J., Boland, W. & Weisser, W. (2007). Real-Time Analysis of Alarm Pheromone Emission by the Pea Aphid (Acyrthosiphon pisum) Under Predation. Journal of Chemical Ecology, 34 (1), 76-81 DOI: 10.1007/s10886-007-9397-8