Sex is more attractive than fear… for insects too!

In the last months I found in literature several very intriguing papers about aphids and their biological control. A good example is the paper entitled “Effect of synthetic and plant-extracted aphid pheromones on the behaviour of Aphidius colemani” recently published by O. M. C. C. Ameixa and P. Kindlmann in the Journal of Applied Entomology.

According to this paper the aphid parasitoid Aphidius colemani (in the photo from the Viridaxis homepage) is sensitive to a mixture of odours including both synthetic and plant-extracted nepetalactone (a component of aphid sex pheromone) and (E)-b-farnesene (aphid alarm pheromone). The behavioural responses of A. colemani to three semiochemical groups with different concentrations were studied in a square arena by Ameixa and Kindlmann showing that parasitoid females were significantly attracted by the semiochemicals, when their concentrations were high, in which case the females spent more time in squares with semiochemicals. However, the majority of females preferred plant-extracted nepetalactone, when it was in high concentration, but they consistently did not respond to (E)-b-farnesene.

These results support previous data showing that a high concentration of (E)-b-farnesene became repellent to the egg parasitoid Chrysonotomyia ruforum and that parasitoid females were not attracted by different concentrations of (E)-b-farnesene, but when this component was offered against a background of a non-attractive natural blend of pine volatiles, the combination became attractive… suggesting as a whole that to be detected by the parasitoid, (E)-b-farnesene must be in a combination with other plant volatiles.

As a whole these results are extremely important considering that some trials with genetically modified plants producing (E)-b-farnesene are in progress (as reported here) using (E)-b-farnesene alone making these plants probably not really effective to fight aphids.

Ameixa, O., & Kindlmann, P. (2012). Effect of synthetic and plant-extracted aphid pheromones on the behaviour of Aphidius colemani. Journal of Applied Entomology, 136 (4), 292-301 DOI: 10.1111/j.1439-0418.2011.01638.x

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Sensing aphids

In most aphid species, the volatile sesquiterpene (E)-β-farnesene (Eβf) is released as an alarm pheromone in response to predation and is also emitted continuously at low levels. Some aphid predators use Eβf as a foraging cue, suggesting that the benefits to aphids of signaling via Eβf must be weighed against the cost of increasing apparency to natural enemies.

At the same time, aphid alarm pheromone has been shown to mediate mutualistic interactions between ants and aphids, in which ants protect “myrmecophilic” aphids while collecting aphid honeydew (a rich source of carbohydrates). Nault et al. (1976) observed that ants became very aggressive in the presence of alarm pheromone and increased their rate of attack on aphid predators, but did not attack aphids. In contrast, when alarm pheromone was applied to colonies of aphid species that are not ant-tended (non-myrmecophilic), ants became aggressive towards the aphids themselves (Nault et al., 1976). More recently, ants’ ability to perceive Eβf was confirmed by Mondor and Addicott (2007).

It was frequently believed that ant-aphid mutualisms were tightly linked, coevolved responses. However, it has been proposed that these dyads may evolve, especially in facultative as opposed to obligate mutualists, as ‘loose relationships’ between species explaining why ants are capable of tending multiple aphid species, either simultaneously or sequentially, in their native habitats. The Argentine ant, for example, is capable of tending many different aphid species in its native environment  and many of these aphids are likely to use E-b-farnesene as their alarm pheromone. Interestingly invasive ants, such as Argentine ant in Europe and USA, may form mutualistic associations with native aphids due to selection for this trait in the ant’s native environment.

The study of aphid-ant interaction will be therefore very useful non only to better understand the interaction between these taxa, but also to improve our knowledge about ant invasive species.

(Photo of Alison Bockoven from the blog 6legs2many).

References

• Mondor, E., Addicott, J. (2006) Do exaptations facilitate mutualistic associations between invasive and native species? Biological Invasions, 9 (6), 623-628 DOI: 10.1007/s10530-006-9062-0
• Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochemistry and Molecular Biology, 42, 155-63 PMID: 22178597.
• Verheggen, F., Haubruge, E., De Moraes, C., Mescher, M. (2009) Social environment influences aphid production of alarm pheromone Behavioral Ecology, 20, 283-288 DOI: 10.1093/beheco/arp009

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Cape fear is still far.. at least for aphids!

A recent post on Scientific American reported that in UK some field trials are in progress studying the effects of a genetically modified  (GM) wheat that should strike fear into aphids and attracts deadly predators to devour them.

The genetically modified wheat emits a pheromone which aphids generally release when they are under attack to create panic and prompt the insects to flee (alarm pheromone). As frequenly occurs in nature, some predators may use the prey chemical communication to locate preys. Similarly, this wheat also attracts some parasitoid wasps to provide a second line of defence for crops since these wasps lay eggs in the aphids killing them.

As you can see in the following video by Christine Woodcock, aphids become agitated and move away  after perceiving the alarm pheromone:

According to this assumption on GM wheat, aphids should move toward other plants… BUT…  according to a paper published some years ago in Ecology Letters (here a summary), aphids were shown to react mainly to the frequency of pheromone release and not the actual quantity present, possibly to avoid manipulation by plants. Thus, to reduce damage caused by aphids, the major insect pests in Europe, it may prove effective to apply pulses of alarm pheromone to infested fields in place of a continuous production. At the same time, a recent paper published in BMC Ecology by Grit Kunert, Carolina Reinhold and Jonathan Gershenzon  provided no support for the hypothesis that plant emission of the aphid alarm pheromone has a direct defense effect against aphids and they suggested that  if plants continuously produce EBF aphids may become habituated. In particular Kunert et al concluded that “the results of this investigation demonstrate that EBF produced continuously by transgenic A. thaliana does not act as a direct defense against aphids. The same conclusion might well be applicable to the continuous emission of EBF from other plants though more studies are necessary. (…) This may be due to the fact these transgenic plants release EBF constantly as opposed to the pulsed release caused by natural enemy attacks on individual aphids. ”

This does not imply that this trial is not interesting at all, since there is scattered evidence in the literature suggesting that alarm pheromone emission might serve as an indirect defense by attracting aphid predators and it will be very interesting to see what will happen to aphid predation. Aphids are ancient pest crop insects and I fear (or as aphidologist I’m sure) that we are at present not near to their debacle.

Reference

Kunert G, Reinhold C, Gershenzon J (2010). Constitutive emission of the aphid alarm pheromone, (E)-β-farnesene, from plants does not serve as a direct defense against aphids BMC Ecology (10)

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