Ants as farmers, aphids in the slow lane

If you grow soft fruit such as currants or gooseberries, you are probably familiar with the sight of numerous aphids densely clustered around the stems, making the leaves wrinkled and deformed. You may also be aware that some ant species 'farm' aphids in order to consume the sugar-rich 'honeydew' that they excrete. However, this is a complex behaviour and so is worth a closer look.

A colony of Aphis schneideri on black-currant Ribes nigrum, attended by black garden ants Lasius niger

First of all, there are numerous aphid species that are found on cultivated fruits, and they can be difficult to tell apart. Those in the photo above are on black-currant Ribes nigrum - within the Ribes-feeding group, only one species has long, acute, erect to semi-erect hairs on the antennae (especially near the base), and that is what is seen here, Aphis schneideri (I couldn't get a clear photo of the antennal hairs, so you'll have to trust me on that). A. schneideri is also commonly associated with R. nigrum, causing clusters of terminal leaves to fold and distort, and the aphids are grey-green, with paler legs and often with a scattered coating of small pale waxy particles.

The ants seen attending the aphids here are the common black garden ant Lasius niger. Not all colonies of L. niger do this, although when it occurs, there is mutual benefit - the ants obtain sugar-rich honeydew and in turn protect the aphids from predators. So far, all straightforward, but exactly how the ants do this was not understood until a few years ago. It has been known for some time that, in order to ensure a dense crop of aphids, ants limit their dispersal (aphids otherwise disperse to new plants when overcrowded, the production of winged forms being triggered by the frequency of contacts between individuals) by biting off their wings (Kunkel 1973) or by secretions from the ants' mandibular glands interfering with the development of winged aphids (Kleinjan & Mittler 1975). Conversely, ants have been seen carrying aphids to suitable, good-quality host plants within their nest's home range. However, aphids also disperse by wandering (which may be more prevalent than dispersal by flying) and some decades ago, both Banks & Nixon (1958) and El Ziady (1960) noticed that the presence of ants seemed to slow aphids down, but no further research was undertaken until Oliver et al. (2007).

Ants are known to lay 'semiochemical' trails by touching glands onto the surface of their substrate, and these chemical marks can lead others from their nest sources of food (Hölldobler & Wilson 1990). Such chemicals can also be applied passively through shedding of cuticular hydrocarbons and this is important recognising nest-mates and, possibly, home-range territories (Devigne & Detrain 2002). Moreover, other insects, including herbivores and aphid predators, have  been found to respond to chemicals that indicate the presence of ants (Offenberg 2004). However, Oliver et al. (2007) found that these ant chemicals had a tranquilising effect on aphids, causing them to walk more slowly and thus - as with the other effects noted above - maintain higher densities which provide the ants with more honeydew.

Although ants have been seen deterring aphid predators such as ladybirds, this does not mean that the mutualistic arrangement is entirely positive for the aphids. Their manipulation by ants means that their dispersal is reduced (or at least delayed) which may have impacts on the wider population (or 'metapopulation') and increase competition between closely packed individuals. Also, dense aggregations may be repeatedly attacked, and sometimes wiped out, by specialist parasitoids which are able to evade ants, such as the small parasitic wasp Lysiphlebus cardui (Weisser & Völkl 1997). Lastly, ants are occasionally seen eating aphids and it appears that this primarily occurs when individual aphids are encountered away from the aggregation. Not only would this prevent aphids being used for the benefit of rival neighbouring ant nests, but presumably produces an evolutionary pressure to 'obey' ant chemical cues rather than be able to avoid the tranquilising effect.

A Lasius niger individual at a colony of Aphis schneideri

So, definitely a more complex story than it initially seemed (isn't it always!), but also a more interesting one, and something you may be able to witness in your own garden. If you are interested in identifying aphids, a standard work covering British Aphidini (the 'tribe' including the genus Aphis) is Stroyan (1984), but be warned - this is not an easy group to identify to species level, and the separation of some species can be uncertain.

References

Banks, C.J. & Nixon, H.L. (1958). Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. Journal of Experimental Biology 35: 703-711.
Collins, C.M. & Leather, S.R. (200). Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality? Ecological Entomology 27: 238-241.  
Devigne, C. & Detrain, C. (2002). Collective exploration and area marking in the ant Lasius niger. Insectes Sociaux 49: 357-362.
El Ziady, S. (1960). Further effects of Lasius niger L. on Aphis fabae Scopoli. Proceedings of the Royal Entomological Society A 35: 30-38.
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Harvard University Press, Cambridge, MA.
Kleinjan, J.E. & Mittler, T.E. (1975). A chemical influence of ants in wing development in aphids. Entomologia Experimentalis et Applicata 18: 384-388. 
Kunkel, H. (1973). Die Kotagabe der Aphiden (Aphidina, Hemiptera) unter Einfluss von Ameisen. Bonner Zoologische Beiträge 24: 105-121.
Offenberg, J. (2004). Evidence that insect herbivores are deterred by ant pheromones. Proceedings of the Royal Society B 271: S433-S435.
Oliver, T.H., Mashanova, A., Cook, J.M., Leather, S.R & Jansen, V.A.A. (2007). Ant semiochemicals limit apterous aphid dispersal. Proceedings of the Royal Society B: Biological Sciences 274: 3127-3131.
Stroyan, H.L.G. (1984). Aphids - Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the Identification of British Insects 2(6): 1-232.
Weisser, W.W. & Völkl, W. (1997). Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae). Journal of Applied Entomology 121: 23-28.