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Parasitoid secretions provoke ant warfare
Subterfuge used by a rare wasp may be the key to an alternative type of pest control.

Insect social parasites are extreme specialists that typically use mimicry or stealth
to enter ant colonies to exploit the rich, but fiercely protected, resources within
their nests. Here we show how a parasitic wasp (parasitoid) contrives to reach its
host, itself an endangered species of social parasite that lives inside the brood
chambers of ant nests, by releasing semiochemicals to induce in-fighting between
worker ants, locking the colony in combat and leaving it underprotected. Four of these
chemicals are new to biology and have the potential to control pest species by inducing
different agonistic behaviours in ants.

Ichneumon eumerus is an endangered hymenopteran parasitoid that is found in
less than 20% of populations of its host, the butterfly Maculinea rebeli 5, which is
listed by the World Conservation Union. I. eumerus females deposit their eggs in
M. rebeli larvae, and their progeny emerge 11 months later as adults from their host’s
pupae. Both stages of M. rebeli inhabit colonies of the ant Myrmica schencki, where
the larvae mimic M. schencki larvae in their behaviour and surface chemistry.
I. eumerus seeks its host by first detecting M. schencki colonies that contain M. rebeli,
and then inducing the fighting that enables it to penetrate nests.

We confirmed that I. eumerus uses agonistic chemicals to provoke M. schencki
(Fig. 1). Empty M. rebeli pupal cases from which parasitoids had already emerged
induced fierce fighting in laboratory ant colonies, as did solvent extracts from these
cases painted onto dummies. In contrast, pupal cases produced no reaction after
being washed in solvent (Fig. 1a, and see supplementary information).

Analysis by gas chromatography with mass spectrometry revealed that these
extracts contained three alcohols and three aldehydes: 0.3 mg ml11 Z-9-icosen-1-ol
(Z-9-C20-ol); 5 mg ml11 Z-9-docosen-1-ol (Z-9-C22-ol); 14 mg ml11 Z-9-tetracosen-1-ol
(Z-9-C24-ol); 0.3 mg ml11 icosanal (Z-9-C20-al); 7 mg ml11 docosanal (Z-9-C22-al); and
20 mg ml11 tetracosanal (Z-9-C24-al). Four of these compounds are new to biology;
the functions of the others (Z-9-C22-al and Z-9-C24-al) were previously unknown.

We synthesized each chemical in the laboratory and presented it to M. schencki
colonies on dummies, either separately or mixed in the relative concentrations found
in the extract. Four chemicals provoked at least one significant response (Fig. 1b, and
see supplementary information). Z-9-C20-ol attracted workers to the dummy and
encouraged them to investigate it, but, having touched it, the ants became aggressive
and ran away, so that they attacked sister ants instead. Z-9-C24-al promoted the
initial investigation and, with Z-9-C24-ol, amplified ant aggression; Z-9-C22-al and
Z-9-C24-ol strongly repelled ants. Mixed together, these chemicals drew ants to the
parasitoid, where, having become aroused to a state of high aggression, they were
quickly repelled. This resulted in three to eight times more attacks (P40.001, n49)
being made on kin ants than on I. eumerus, the stimulator of the aggression.

The controlled propagation of alarm plays a key part in ant societies, casting a
social ‘immune barrier’ around them and affording workers instant recognition of
nestmates and discrimination against foreigners. Most of the pheromones involved
in this process are volatile, short-chain hydrocarbons, which allow the rapid expansion
and dissipation of alarm. Only the slave-making ant Formica subintegra, whose
C12–C16 aldehydes are the most persistent and longest-chain semiochemicals known to
provoke ants, has been found to use alarm in the same way as I. eumerus to raid other
ants’ nests. The allomones used by I. eumerus are more persistent still, provoking
aggression for 50 days after secretion.

Our bioassays induced only 56–79% of the ferocity unleashed by a living parasitoid5.
This may be due to the small size of our test colonies — larger ones reacted
more strongly (r 2492%, P40.04, n45), which supports our observation that the
ants themselves amplify and propagate a sense of panic after contact with the wasp,
creating a chain reaction of in-fighting across their society.

No other known secretion enables an individual insect to immobilize up to 80%
of an ant colony. The strength and persistence of this reaction suggests that similar
cocktails of long-chain hydrocarbons might provide an alternative to the use of poisons
and repellents to control pest ants10. If so, this would be an unexpected benefit of
studying obscure taxa11 — sadly, just four unprotected European meadows now support
all of the I. eumerus individuals found in recent decades.