Suicide aphids

Suicidal aphids? Yes, but it's not due to severe depression or panic about falling share prices. Aphids commit suicide for two main reasons - defence against predators and repairing their home.

1a. Defence against predators (part 1)

Ladybird larvae are voracious predators of aphids, and with some aphids living in colonies inside plant galls, such a group would seem like the perfect source of prey. However, researchers (Kazana et al. 2007) have found that cabbage aphids Brevicoryne brassicae can deploy pungent mustard oil 'bombs' - this can kill their enemies but almost always kills the aphid as well. However, the sacrifice is for the greater good of the colony...

The aphids, which feed on plants of the cabbage family, consume chemicals called glucosinolates (such as sinigrin). These are stored in the insects' blood and, when needed, react with the enzyme myrosinase to produce the mustard oil explosion - a chemical reaction producing several toxic products including allyl isothiocyanate, which is the substance giving mustard and horseradish their powerful sinus-clearing flavours. As allyl isothiocyanate is also harmful to the plant, the reactive chemicals are stored in separate places - then, a wound inflicted by a feeding animal mixes the two chemicals and triggers the toxic chemical explosion. Some caterpillars have evolved methods of neutralising this defence such as proteins that inactivate or destroy the glucosinolates. However, B. brassicae ingests the substance, effectively co-opting the plant’s defence. Like the plant, the two reactants have to be stored separately - in the case of the aphid, the myrosinase enzyme is stored in the muscles of the head and thorax - the two only mix when blood and muscle are forced to interact, such as when a predator bites. Watch this video to see aphid defence against a ladybird larva.

Soldier aphids defending against a predatory lacewing.

The enzyme is produced throughout the aphid's life, and is even found in the youngest embryos. The aphids are however almost entirely dependant on plants for glucosinolates; although mother aphids give donate a small amount of sinigrin to their larvae from their abdomens, the larvae have to subsequently seek their own. Beyond that, it is the youngster’s responsibility to get more for itself.

Kazana's research found that the chemical spray was toxic to ladybirds, which subsequently failed to develop into adults and died. The toxin was 100% fatal when delivered by wingless aphids, but the species develops both wingless and winged forms, and ladybirds that attacked winged aphids were only killed around 17% of the time.Analysis showed that winged aphids simply excreted any sinigrin that they ingested, possibly because storing the chemical costs a considerable maount of energy which is unnecessary when they are able to fly away to avoid predators.

So, why do the wingless aphids sacrifice themselves? Well, aphids reproduction is mainly asexual, hence a colony essentially consists of clones - so, with several hundred genetically identical relatives, it is worth one aphid dying to protect the colony.

1b. Defence against predators (part 2)

Toxic explosions aren't the only suicidal methods employed by aphids to protect their colonies. When aphids of the species Quadrartus yoshinomiyai are attacked by a predator (again, such as a ladybird larva), they leave the gall in numbers and grip the jaws and legs of the attacker. They then secrete a waxy liquid which quickly solidifies and glues the ladybird to the plant. Unable to move or bite, the ladybird dies and the aphids die with it. Watch this video to see the result of prodding one of these aphids.


However, the story is a little more complex. Uematsu et al. (2010) found that all the suicidal gluers were effectively menopausal, being the parents of the other aphids in the gall but too old to reproduce again; their role is now defence of the colony and their young. These wingless adults tend to cluster around the exit holes - when present, only 23% of ladybirds were able to penetrate the gall, without them, 64% of attacks were successful.

2. Repairing their home


Many species of aphids are gall-causers, stimulating their host plants to form hollow chambers. These species tend to show cooperative and social behaviour, much like a simple version of the colonies formed by ants and termites. They have specialised ‘soldiers’ who defend the colony, repairing the gall and keeping it clean. As with the chemically-enhanced defenders described above, this can take the form of a suicidal response. Some do this at the cost of their own lives. Kutsukake et al. (2009) found that the gall aphid Nipponaphis monzeni uses 'suicide plasterers', specialised sterile soldiers that repair holes in the gall by leaching their own bodily fluids onto damaged areas, mix it with their legs and plaster it over the hole. The fluid quickly sets and within an hour, the gap is filled, although the process kills the plasterer. Over time, the regenerating plant tissues lift and engulf the aphid 'scab' which eventually disappears. It is not known exactly how the process works, though it appears that the aphids are at least partly responsible for the repair as well as the initial temporary fix, possibly using additional fluids to prevent the scab from dropping off too soon.


The process does however appear similar to wound repair in humans i.e. the clotting fluid hardens to form a scab which provides a temporary seal, giving surrounding plant cells time to repair the damage. This plastering is of key importance - where repair is halted, 92% of galls died within a month, but wheer repairs were completed, only 18% died. while 82% of those that were completely repaired were still around. The plasterers are particularly important in spring, when galls are young, thin-walled and vulnerable.

There are still more questions for research to investigate:

• Do the soldiers actively trigger the chain of molecular events that leads to clotting before they discharge their fluids?
• How do the plasterers tell the plant to fix the injuries - do they inject hormones and other chemicals into the plant with their piercing mouthparts? Possibly, as this may be how gall growth is induced, and some soldiers can inject enemies with toxic enzymes.
• Another social aphid, Pemphigus spyrothecae, repairs gall holes, but without the suicide tactics of N. monzeni. This does mean that repairs take much longer, but why is a faster fix so important to N. monzeni? It may be because their galls are much larger with thousands of individuals, while in other species, colonies number in the mere hundreds. If this is the reason, it may be that colonies need to be very large in order to justify the costly tactic of suicide-plastering. 

References

Kutsukake, M., Shibao, H., Uematsu, K. & Takema Fukatsu, T. (2009). Scab formation and wound healing of plant tissue by soldier aphid. Proceedings of the Royal Society B 276: 1555-1563.

Kazana, E., Pope, T.W., Tibbles, L., Bridges, M, Pickett, J.A., Bones, A.M., Powell, G. & Rossiter, J.T. (2007). The cabbage aphid: a walking mustard oil bomb. Proceedings of the Royal Society B 274: 2271-2277.

Uematsu, K., Kutsukake, M., Fukatsu, T., Shimada, M. & Shibao (2010). Altruistic Colony Defense by Menopausal Female Insects. Current Biology 20(13): 1182-1186.

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Thank you to Mayako Kutsukake and the National Institute of Advanced Industrial Science and Technology (AIST).