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When it rots, it stinks!

Microbes make chemicals that "protect" their food from being eaten by animals like the crab.About 30 years ago, ecologist Dan Janzen bought an avocado in Costa Rica, but the thing rotted before he got to sample it. An annoyed Janzen quickly turned misfortune into fortune by proposing an ecological theory for the awful perfume that bacteria and fungi confer to rotting food: "It is my hypothesis that microbes are often under strong selection to render seeds, fresh fruit, or carcasses as objectionable or unusable to larger organisms as is possible in the shortest period of time," he wrote (see "Why Fruits Rot ..." in the bibliography).

Janzen suggested that the toxins, antibiotics and the gross aromas made by decay organisms were not accidental, but rather the outcome of an evolutionary process that keeps rotting food available to the decomposing organisms. Janzen did not discuss fish, but he suggested that if bacteria and fungi put up a hideous stink, they could hoard the premium filets of dead fish without interference from many live crabs, fish or other animals.

It was a reasonable idea, says Mark Hay, a professor of biology who studies chemical communication in the sea at the Georgia Institute of Technology, but it was not rigorously tested until Hay and a research team including graduate students Deron Burkepile, John Parker and Brock Woodson studied the response of stone crabs to rotten fish.

Big crab stretched out, showcasing it's menacing black-tipped claws
The stone crab steers clear of rotting meat. Photo: Courtesy Mark Hay

Rotten truth
Here's what they did: The researchers baited some crab traps with fresh menhaden, a common bait fish in the Atlantic, and some with menhaden that had rotted for two days in the presence of microbes, and found that they captured many more consumers in the traps with fresh meat. This indicated that the fresh meat smelled more attractive and caused many more consumers to enter those traps.

When the researchers turned their attention to feeding choices, they found that the major crab species in the traps ate 2.4 times as much fresh fish as rotten fish.

In other words, the stench of rotten fish caused the crabs to turn up their noses (assuming they got 'em).

By itself, that didn't prove much. Maybe the crabs disdained the "aged" texture of day-before-yesterday's menhaden. Maybe the unappealing "mature nose" of the menhaden was not due to the bacteria.

Those are legit maybes, but two further tests fingered bacterial vapors that repel. First, fish that had been simmered in antibiotic water, and therefore lacked bacteria, was just as appealing as fresh fish. Second, when the researchers extracted organic chemicals from their fish broth and put them on fresh menhaden, those fish were just as repellent as rotten fish.

recipe card for 'Fetid Fish'

And now the story gets gruesome. How bad was the stench when the scientists concentrated the chemistry of the rotten fish? We suggested the back-side of a filthy fishing dock, but Hay assured us this was like comparing a guppy to a blue whale. Grinding up rotten fish and pouring chemicals over them is not for wimps, he said. "The three guys who worked on this the most quit bathing because it didn't help. They stank so bad that nobody would work with them. They were dedicated scientists, but were not very high on the girls' hit list."

Unfortunately, although the researchers proved that the crabs were responding to some bacterial chemical, even after a year's stench-rich toil, they could not identify exactly which chemical was protecting fetid fish from crab claw.

White fish aglow with health and a rotted fish you can smell from here
Top: this fresh fish is a stone crab's delight. Bottom: A half-rotten fish is not. Photo: Courtesy John Parker

Rotten shame
Chemicals may seem a crude channel for communication, but Hay stresses they are the rule, not the exception. "Most living things don't have eyes or ears, so their communication is chemical. If something shows up next to them, they sense it chemically; they run, eat or mate based on chemicals." A homo-centric view of ecological interactions isn't enough, he says. "When we look at ecosystems, we are very limited if we look only through our own senses."

Once we see that bacteria on rotting fish causes many crabs to order from a different menu, the evolutionary advantage of making a stench becomes obvious. Bacteria tend to survive if "their" fish isn't eaten by a crab or a live fish.

If we look at the equation from the other side, it's also obvious that multi-cellular organisms have an interest in shunning the polecat perfume of putridity: Rotten food can carry dangerous pathogens.

So which is it, Hay asks? "Is this evolution on the part of the animal to avoid something that's bad, or is it evolution on the part of the microbe to sequester resources?"

In fact, both the bacteria and the animals may be evolving in a direction that leaves the fetid food to the bacteria. "It is to our advantage not to eat things that will make us sick, so we should have evolved to avoid them," says Hay. "It's also to the microbe's advantage to quickly make us think, 'I don't want to eat that,' and leave the food to the microbe."

Two men cruise around blue water with large mesh pens full of flesh
All in a day's work: letting meat rot, and feeding it to stone crabs. This is seriously stinky work, so a fresh breeze is always welcome! Photo: Courtesy Mark Hay

Overall, Hay hopes the study will help ecologists appreciate bacteria as active players in food webs, rather than inert decomposers. "We wanted to cue ecologists in to the fact that the microbes are not just non-responsive gorp on the bottom, they are actively grabbing resources."

— David Tenenbaum

• Chemically Mediated Competition Between Microbes and Animals: Microbes as Consumers in Food Webs, Deron E. Burkepile Et Al, Ecology, Nov. 1, 2006.

• Why Fruits Rot, Seeds Mold, and Meat Spoils, Janzen, D. H. 1977, American Naturalist 111:691-713.

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