Facultative slave-making ants tolerate alien slaves but not their masters

A blog post highlighting the article written by Włodarczyk in Insectes Sociaux

Written by Tomasz Włodarczyk

Many ant species in nature are closely associated with other ant species. The closest form of such an association is called a mixed colony where ants of both species inhabit common nest, share food and raise their brood side by side. Mixed colonies arise as a result of social parasitism when one species exploits the labor of the other, such as in slave-making ant species. Slave-maker ants raid the nests of the host species, steal the pupae and bring them back to their home nests. Newly-emerged individuals integrate into the parasite’s society and perform all domestic duties.

In the lab, we can also create mixed colonies using species that would never form such an association in nature. The species don’t even have to co-exist geographically. This is because ants learn (imprint) colony odor after eclosion from pupae and use it as a template for subsequent nestmate recognition. Thus, by putting together callow ants of different species we can create a mixed colony of individuals that have imprinted on the odor of each other.

As a part of my PhD project I investigated the recognition behavior of ants using a colony of the facultative slave-making ant species, Formica sanguinea. By supplying them with pupae of Formica polyctena or F. rufa -which soon emerged- I formed mixed colonies (Włodarczyk 2012, Włodarczyk and Szczepaniak 2014). These experiments were inspired by the studies conducted by Wojciech Czechowski (1994) whose results suggested that F. sanguinea ants acquire their recognition signature form their slaves, as in the obligate slave-making species Polyergus samurai (Yamaoka 1990).

Excavation

Formica sanguinea is a facultative slave-making species enslaving ants from the subgenus Serviformica. Here, a colony with black F. fusca slaves has been excavated.

Later I became curious about how things look in the case of F. sanguinea colonies containing the most frequently used slave species, F. fusca. Results of chemical studies revealed that odor of F. sanguinea ants is quite different from that of its host species (Martin et al. 2008, Włodarczyk and Szczepaniak in prep.). Moreover, we found that enslaved F. fusca ants develop a chemical recognition signature which is intermediate between that of their parasite and ants from free-living colonies (Włodarczyk and Szczepaniak in prep.). This raised the question about how recognition cue diversity in F. sanguinea colonies affect the recognition abilities of ants. Even more interesting was whether there are differences in the recognition abilities between F. sanguinea and F. fusca ants given that the parasite is the only party to be under selective pressure to live in such a condition.

I collected eight queenright F. sanguinea colonies containing F. fusca slaves and maintained in the the laboratory. The slave-making F. sanguinea ants and their slaves were exposed on a Petri dish to anesthetized ants from alien colonies. I measured the number of aggressive behaviors in various encounter combinations. I showed that F. sanguinea ants are able to discriminate other individuals from the same species from alien colonies towards which they exhibit aggressive behavior. However, slaves from alien colonies were generally tolerated. This result supports the hypothesis that F. sanguinea ants are intrinsically tolerant to individuals whose odor indicates that they are slaves. Otherwise slave-making ants might accidentally attack their own slaves, which possess a recognition signature that deviates from that of the other slaves. This situation would arise when slaves from new source colony appear in the slave-maker’s society.

The other result was that slaves (F. fusca) are poor at discriminating slave-making ants and slaves from alien colonies and do not exhibit an overt aggression toward them. This could be explained by the high within-colony recognition cue diversity that hampers formation of an accurate template during colony’s odor learning phase. This is intuitive explanation since it might be hard to recognize an object of a given class when this class is relatively heterogeneous. Thus, there is no recognition barrier for F. sanguinea ants to take over slaves from alien colonies. However, such a phenomenon has not been recorded for F. sanguinea ants. Therefore we can hypothesize that intraspecific raids play at best very limited role as a way of slave gaining.

Formica

Formica fusca slaves showing aggressive behavior towards an anesthetized conspecific ant.

Moreover, I conducted an experiment in which slaves and slave-makers were reared separately. After about 2-month period, ex-slaves elicited aggression in ants from stock colonies (both in slave-makers and in slaves). Conversely, slave-makers separated from slaves were still treated as nestmates. This result suggests that F. sanguinea exert a strong impact on the odor of F. fusca ants, possibly by the transfer of recognition cues during food exchange.

The results of my study highlight that selective pressures associated with different life histories can lead to differences in recognition systems between social insect species.

 

References

Czechowski W (1994) Impact of atypical slaves on intraspecific relations in Formica sanguinea Latr. (Hymenoptera, Formicidae). Bull Pol Acad Sci 42(4):345–350

Martin SJ, Helantera H, Drijfhout FP (2008) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol J Linn Soc 95:131–140

Włodarczyk, T (2012) Recognition of individuals from mixed colony by Formica sanguinea and Formica polyctena ants. J Insect Behav 25: 105–113

Włodarczyk T, Szczepaniak L (2014) Incomplete homogenization of chemical recognition labels between Formica sanguinea and Formica rufa ants living in a mixed colony. J Insect Sci 14:214

Yamaoka R (1990) Chemical approach to understanding interactions among organisms. Physiol Ecol Japan 27:31–52

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