The Scent of Fear – the aphid alarm pheromone

We are all familiar with the effects of epinephrine (adrenaline) and norepinephrine (noradrenaline) on us when placed in a position of stress, such as public speaking or even worse danger.  We flush, shake, our heart rate accelerates and many of us we begin to sweat profusely, thus visibly advertising our distress; sometimes embarrassingly so

 

if we have an antiperspirant  fail and happen to be wearing a dark shirt.

http://www.silkyskin.co.uk/blog/wp-content/uploads/2012/07/man_giving_speech.jpg

Those seeing these symptoms may feel a degree of sympathy for the victim, but do not usually flee the scene, although they may sometimes feel tempted to do so.

The case with aphids is very different.   Aphids, when perceiving a threat to their neighbours by a predator or parasite, flee the scene rapidly, by flight, if winged, on foot if not, or even by leaping from their host-plant to the ground below.  The pea aphid, Acyrthosiphon pisum walks away or drops from their plant (Clegg & Barlow, 1982) as does the rose-grain aphid, Metopolophium dirhodum (Larsen, 1988).  This may seem a risky move since it seems that about 10% of all aphids that fall from their host plant don’t manage to get back (Sunderland et al., 1986), but for a clonal organism the risk is obviously worth it.

So how does this communal fright and flight response come about?  Most aphids have a pair of siphunculi or cornicles at the rear of their abdomen.  These vary in size and shape, in some aphids being long and slender, in others short and stubby and in yet others reduced to a shallow indentation (pore) or in a few species, totally absent.

The role of aphid siphunculi has been debated since the days of Linneaus and Reaumur who considered them to be the source of honeydew (Hottes, 1928).  Hottes himself in a comprehensive review of the various theories put forward for the function of the siphunculi, dismissed the defence theory of Busgen (1891) and plumped for an excretory role, although he did suggest that volatile substances were produced by the siphunculi in addition to the waxy visible drops.    By the middle of the last century it was generally accepted that the siphunculi were involved in defence, but in a purely physical way, in that the waxy exudate was used to deter or disable the attacking predators or parasites (e.g. Dixon, 1958; Edwards, 1966).  At about the same time, the chemical composition of the visible exudate was confirmed as being primarily triglycerides with myristic acid being the major fatty acid present (Strong, 1966).

Aphis nerii siphuncular exudate.  http://springfieldmn.blogspot.co.uk/2014/08/aphid-cornicles.html

 

 

Hawthorn-parsley aphid Dysaphis apiifolia producing sipuncular exudates whilst under attack by a parasitic wasp.  Many thanks to Tom Pope for permission to use this clip.

In 1968 an alarm pheromone was identified and isolated from the cotton stainer, Dysdercus intermedius (Calam & Youdeowei, 1968) so it was not surprising that attention should be focused on aphids, many of which show a similar group dispersive behaviour when a predator approaches them.   The aphid alarm pheromone (E)-β-farnesene was, however, not formally identified until  1972 (Bowers et al, 1971), although Maria Dahl had demonstrated the  previous year that a solution made from crushed aphids would cause an alarm response in other aphids of the same and different species (Dahl, 1971). Unsurprisingly, as during the 1970s and 1980s scientists from the USA were notorious for only citing papers written in English, Bowers et al. (1972), failed to cite her in their paper, instead citing two other American authors (Kislow & Edwards, 1972).

This discovery resulted in a flurry of papers from around the world as insect physiologists vied to be the first to isolate alarm pheromone from different aphid species (e.g. Weintjens et al., 1973; Montgomery & Nault, 1977; Wohlers, 1980).  There were also more ecological studies such as that examining the way alarm pheromone in ant-attended aphids enhances the relationship between them and their ant farmers (Nault et al., 1976) thus acting as a synomone (Nordlund & Lewis, 1976).  As time has gone on the interest in aphid alarm pheromone has remained unabated with new twists and surprises being discovered.  For example, as well as stimulating the escape response, the alarm pheromone also stimulates those surviving pea aphids to produce winged offspring thus facilitating future long-distance dispersal away from the predators (Kunert et al., 2005).  Aphid alarm pheromone can also act to help natural enemies find their aphid prey (e.g. Micha & Wyss, 1996), in this case acting as a kairomone.

The use of sex pheromones in integrated pest management is well established (Witzgall et al., 2010) and works very effectively in most cases. More recently, researchers at Rothamsted Research have courted controversy by trialing GM wheat that has been engineered to produce aphid alarm pheromone.  Many entomologists, including me, although finding the concept (Yu et al., 2012) interesting, doubt that it will work in a field situation.  I can certainly see a role for using alarm pheromones as an alternative to conventional chemical control of insect pests and it will be interesting to see if it will prove as effective as using sex pheromones.

 

References

Bowers, W. S., Nault, L. R., Webb, R. E. & Dutky, S. R. (1972). Aphid alarm pheromone: isolation, identification, synthesis. Science 177, 1121-1122.

Busgen, M. (1891)  Der Honigtau. Biologische Studien an Pflanzen und Pflanzenläusen.  Jenaische Zeitschrift für Naturwissenschaft, 25, 339-428

Calam, D.H. & Youdeowei, A. (1968) Identification and functions of secretion from the posterior scent gland of fifth instar larva of the bug Dysdercus intermedius. Journal of Insect Physiology, 14, 1147-1158

Clegg, J.M. & Barlow, C.A. (1982) Escape behaviour of the pea aphid, Acyrthosiphon pisum (Harris) in response to alarm pheromone and vibration. Canadian Journal of Zoology, 60, 2245-2252.

Dahl, M. L. (1971). Über einen Schreckstoft bei Aphiden. Deutsche Entomologische Zeitschrift 18, 121-128.

Dixon, A. F. G. (1958). The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London,110, 319-334.

Dixon, A. F. G. (1958). The protective function of the siphunculi of the nettle aphid, Microlophium evansi (Theob.). Entomologist’s Monthly Magazine, 94, 8.

Edwards, J.S. (1966) Defence by smear: supercooling in the cornicle wax of aphids.  Nature,  211, 73-74.

Hottes, F. C. (1928). Concerning the structure, function, and origin of the cornicles of the family Aphididae. Proceedings of the Biological Society of Washington 41, 71-84.

Kislow, C.J. & Edwards, L.J. (1972)  Repellent odour in aphids.  Nature, 235, 108-109.

Kunert, G., Otto, S., Rose, U.S.R., Gershenzon, J., & Weisser, W.W. (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters, 8, 596-603.

Larsen, K.S. (1988) Responses of different age classes of the rose-grain aphid, Metopolophium dirhodum (Wlk.) to attack by a simulated predator.  Journal of Applied Entomology, 105, 455-459.

Montgomery, M. E. & Nault, L. R. (1977). Comparative response of aphids to the alarm pheromone, (E)-B-farnesene. Entomologia experimentalis et applicata 22, 236-242.

Micha, S.G. & Wyss, U. (1996)  Aphid alarm pheromone (E)-B-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidinae).  Chemoecology, 7, 132-139

Nault, L. R., Montgomery, M. E. & Bowers, W. S. (1976). Ant-aphid associations: role of aphid alarm pheromone. Science 192, 1349-1351.

Nordlund, D. A. & Lewis, W. J. (1976). Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. Journal of Chemical Ecology 2, 211-220.

Strong, F.E. (1966)  Observations on aphid cornicle secretions.  Annals of the Entomological Society of America, 60, 668-673.

Sunderland, K.D., Fraser, A.M., & Dixon, A.F.G. (1986) Field and laboratory studies on money spiders (Linyphiids) as predators of cereal aphids. Journal of Applied Ecology, 23, 433-447.

Wientjens, W. H., Lakwijk, C. J. M., & Van Der Marel, T. (1973). Alarm pheromone of grain aphids. Experientia, 29, 658-660.

Wohlers, P. (1980). Die fluchtreaktion der erbsenlaus Acyrthosiphon pisum Aausgelöst durch alarmpheromon und zusätzliche reize. Entomologia experimentalis et applicata 27, 156-168.

Witzgall, P., Kirsch, P. & Cork, A. (2010) Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36, 80-100.

Yu, X.D, Pickett, J., Ma, Y.Z., Bruce, T., Napier, J., Jones, H.D. & Xia, L.Q. (2012)  Metabolic engineering of plant-derived (E)-β-farnesene synthase genes for a novel type of aphid-resistant genetically modified crop plants.  Journal of Integrative Plant Biology, 54, 282-299.

 

Post Script

A brief guide to mones

An allomone is any chemical substance produced and released by an individual of one species that affects the behaviour of a member of another species to the benefit of the originator but not the receiver e.g. the ability of some plants to release aphid alarm pheromen and thus deter aphids form landing on them.

An apneumone is any substance produced by nonliving material that benefits a recipient species but is detrimental to a different species associated with the non-living material

A kairomone is a semiochemical, emitted by an organism, which mediates interspecific interactions in a way that benefits an individual of another species which receives it, without benefiting the emitter.  For a detailed critique of the term kairomone see Ruther et al. (2002).

A pheromone is a secreted or excreted chemical factor that triggers a social response in members of the same species. Pheromones are chemicals capable of acting outside the body of the secreting individual to impact the behaviour of the receiving individual e.g. alarm pheromones, food trail pheromones and sex pheromones.

A synomone is a substance produced by an individual of one species that benefits both the producer and the recipient which is of a different species.  An example is the release of chemical elicitors by plants that attract entomophagous insects when they are attacked by herbivores.