David M. Wilkinson
Liverpool John Moores University, UK
An ecologist enjoys a smelly experiment on a neglected link in the food web.
I have long been fascinated by an idea from the 1970s about rotting food. Daniel Janzen, now at the University of Pennsylvania in Philadelphia, suggested then that many of the noxious chemicals secreted by microbes in decaying food are produced to fend off large animals, allowing the microbes to keep the resource for themselves.
It's an intuitively appealing hypothesis. Our own experience is to be repulsed by putrid food, and several studies have shown that birds prefer fresh over rotted fruit. Most recently, a careful study in the seas off the southeasten United States provided further support for Janzen's idea (D. E. Burkepile et al. Ecology 87, 2821–2831; 2006).
In what must have been a gloriously smelly experiment, the researchers baited crab traps with dead fish, either rotten or fresh. The microbe-laden carrion was four times less likely to be consumed by scavengers than the fresh fish.
This provides clear evidence that microbes compete for food with larger animals, something that has been largely overlooked in the huge ecological literature on food webs and feeding relationships. But it doesn't tell us how the chemicals evolved.
Last year, I published with colleagues a theoretical analysis of the evolutionary implications of Janzen's idea (T. N. Sherratt et al. Ecol. Modell. 192, 618–626; 2006). Our model suggested that the chemicals cannot have evolved solely to protect against large animals, because the temptation for microbes to 'cheat' by free-riding on toxin production by others undermines the system.
The experiments done by Burkepile et al. show that the effect is real, but perhaps these chemicals first evolved for other reasons, such as inter-microbe competition?

Comments
One may wonder how the multitude of carrion loving insect species that not only are attracted to rotting food but also depend on it for their nourishment and/or reproduction fir into Janzen's theory. Attraction to decomposing flesh in insects has been such successful evolutionary strategy that several species of plants have evolved chemicals smelling like rotting flesh, e.g. Titan arum and Rafflesia, to attract carrion loving insects for pollination.
Is it plausible that the fact that putrid smells attract insects rather than discourage them could indicate that there is less (or no) competition between microbes and insects?
Posted by: Mario Pineda-Krch | June 5, 2007 04:49 AM
Although I find Janzen’s idea fascinating my modelling work (mentioned in my Journal Club essay) leaves me sceptical that these chemicals have evolved for the reasons Janzen suggests. However, in relation to insects I can see several points which could be used in defence of his idea.
1/ Invertebrates can evolve to detoxify chemicals produced to deter them. For example the caterpillars of the Cinnabar Moth (Tyria jacobaeae) have not only evolved counter measures to toxins produced by their food plant, they even put these chemicals to use in their own defence.
2/ Vertebrates may be a greater threat to the substrate used by microbes than are invertebrates as they have a larger bite size – so potentially removing more substrate. I have used similar arguments in suggesting that vertebrates may be a greater selection pressure than invertebrates in the evolution of poisonous fungi (American Naturalist 166, 767-775.), as a single bite by a deer can destroy a whole fruiting body while invertebrates often do much less damage. So microbes may mainly be targeting vertebrates with these chemicals.
Posted by: David M Wilkinson | June 5, 2007 01:18 PM