Smell, not sight, guides fly and wasp flower selection (or why stinky flowers attract flies)

Picture this: a luscious green mountain range littered off and on with flowers of every type. Lower in the mountains is green vegetation, higher up are grasslands. Eucomis, or pineapple lilies, have a striking, colorful appearance and grow at varying altitudes along the mountainside. But there tends to be one surpising difference: Two species of the higher altitude pineapple lilies have, not the delicate scent of coconut as do some of the other species, but the much more alarming scent of carrion.

This is a textbook example of adaptation, or more specifically, fragrance evolution in flowers and its role in pollinator selection. A recent study published online in Proceedings of the Royal Society Biology looked closely at carrion flies and pompilid wasps and the respective Eucomis species that they pollinate in South Africa’s Drakensberg mountain range.

The scientists found that the flies selected particular species of pineapple lilies over others as determined by the strength of the flowers’ sulfur composition. That is, the fly Sacrcophaginae, commonly called a carrion fly, pollinated the sulfur-carrying flowers Eucomis humilis and Eucomis bicolor. This is compared to the wasp species Hemipepsis capensis, a pompilid wasp, which pollinated the sulfur-free Eucomis autumnalis and Eucomis comosa.

To determine that the flies were  attracted to the sulfur composition and not to other factors—such as the color or nectar abundance of these particular flowers—the researchers added a one-to-one blend of dimethyl disulfide and dimethyl trisulfide to the wasp-pollinated (and fly-deterrent) pineapple lily species. The flies found the sulfur-enhanced flowers just as attractive as the stinkier lily species they normally pollinated.

But why did some pineapple lilies develop this stinky attribute while others have a delicate, sweet scent? The researchers propose that a mutant wasp-pollinated Eucomis began producing the sulfur compounds some time ago; as a result, fly pollinators were attracted to the scent and began unintentionally spreading the pollen of the malodorous strain. In addition, fly-pollinated pineapple lily species are more prevalent in high altitude grasslands of the region than the wasp-pollinated species, said the authors. This suggests flies could be the most accessible type of pollinator for flowers growing at higher elevations.

And since carrion flies are predisposed to the distinct odors of decay, they would also be attracted to the sulfides found in E. humilis and E. bicolor (this is the case with oligosulfides, the volatiles of a particularly smelly plant stapeliae that also mimics the scent of carrion). Naturally, a carrion-smelling flower would have better reproductive success in an area abundant with flies.

This still leaves one important question:  If the pollinators select a flower based on its scent, why do pineapple lily species also have unique coloration? As the researchers explained: “Although showy to the human observer, Eucomis flowers are cryptically colored and likely do not stand out from the background vegetation in the eyes of their pollinators.” This is true even in the case of wasps, which can locate pineapple lilies that are completely hidden from view by scent alone.

However, in the eyes of other insects, said the researchers, the coloration of these flowers looks unattractive. They suggest that this is probably a defense mechanism of the pineapple lily: “The costs of pollen loss to unfaithful floral visitors may be the basis for the evolution of this cryptic coloring.”

So to the pollinators, these flowers may not be particularly pleasing to the eye, but they have an irresistible scent—the basis for a mutual attraction needed for the flower’s reproductive success. For other insects, these flowers do not appeal by look or by smell. And to the human observer, these pineapple lilies may be visually pleasing, but they are probably not worth stopping to smell.

Drakensberg: http://www.flickr.com/photos/arnolouise/ / CC BY-NC 2.0

Eucomis bicolor: http://www.flickr.com/photos/ericinsf/ / CC BY-NC-ND 2.0

Eucomis autumnalis: http://www.flickr.com/photos/petrichor/ / CC BY-NC-ND 2.0

Shuttleworth, A., & Johnson, S. (2010). The missing stink: sulphur compounds can mediate a shift between fly and wasp pollination systems Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2010.0491