Have you ever bitten into a rotten apple and thrown it away in disgust? Some scientists think that was microbes waging biological warfare against you—and winning. The idea, almost 40 years old but never properly tested, argues that bacteria and fungi actively spoil food to keep large animals, like humans, from taking away their meal. Now, a new paper bolsters that case with a mathematical model, proving that the old hypothesis is still fresh.
Ecologist Daniel Janzen, then at the University of Michigan, Ann Arbor, first proposed the idea in a 1977 paper , which he wrote was "inspired by paying 95 cents for a rotten avocado." Microbes, he argued, don't just happen to spoil food when they gorge on it; they have evolved to make it unappetizing to large animals as fast as possible—for instance by producing bad-tasting compounds—so they can keep the meal to themselves. "Fruits rot, seeds mold, and meat spoils because that is the way microbes compete with bigger organisms," he wrote. (He also hypothesized that plants, which benefit from animals spreading their seeds, may have developed countermechanisms such as producing chemicals to repel fungi and bacteria.)
Some researchers have gone to great lengths to see whether the idea actually holds true in nature. In one experiment, U.S. scientists baited crab traps off the coast of Georgia  with fresh or rotten fish and found that fresh carrion attracted almost three times as many animals, showing that "bacteria compete with large animal scavengers by rendering carcasses chemically repugnant," according to the study. Other experiments have shown that birds prefer fresh fruits to rotten ones.
But in 2006, four scientists tried to build Janzen's theory into a mathematical model  and ran into trouble. They found that if microbes put extra work into spoiling the food for large animals, they would be outcompeted by others that did not bother. Janzen's idea sounded plausible but was unlikely to be true, they concluded. The disgusting taste of a rotten apple, in their view, was more likely an accidental byproduct of its breakdown by microbes.
Now, some of the researchers who built that earlier model have revisited the topic, but they changed a key assumption: "In our original model pretty much any microbe could arrive anywhere," says David Wilkinson, an ecologist at the Liverpool John Moores University in the United Kingdom and one of the authors. That meant that any rotting fruit would likely be colonized by all kinds of microorganisms. In that scenario, microbes that evolved to spoil food would always be outcompeted by microbes that just reaped the benefits without investing in spoiling the food themselves. "In the new model they do not move quite as easily and that is the crucial biological difference." The new model predicts that "even in the extreme case where there is a very high cost to spoilage … spoiling microbes can be sustained ," the authors write online today in the Proceedings of the Royal Society B.
In essence, the old model viewed rotting fruit as a buffet with all kinds of microbes in attendance, explains Michael Kaspari, a biologist at the University of Oklahoma, Norman, who was not involved in the work. "The poisoner, taking the time to [spoil the food for large animals] while everybody else is stuffing their mouths, gained little advantage," he writes in an e-mail. "The new model allowed for the more realistic possibility that if the poisoner gets to the party first, it can keep everybody else at bay. As long as there are enough parties, poisoners prosper."
Experiments are still needed to back up the assumptions of the new model, Wilkinson cautions. He suggests that biologists should try to track which microbes arrive on a fruit or a dead animal over time. "With birds you would just sit there with a pair of binoculars and see what turns up," he says. "With microbes it is not that easy, but it is not entirely impossible with molecular methods."
Even then, however, it will be hard to prove that microbes are actually targeting large animals; they could also be trying to repel other microbes, Kaspari argues. "To a microbe busily rotting a banana, do we even exist?"
Janzen, who now works at the University of Pennsylvania, says he is happy that his idea has been converted into a plausible model. But he doesn't really need mathematics to know he is right. "Have you ever bitten into a piece of moldy bread or a spoiled orange, to say nothing of over-ripe fish?" he writes in an e-mail. "How much theory did you need for your reaction? Who won?” But whatever his reservations, the research is worthwhile, Janzen says. "It is good to have people exploring the interactions between microbes and us big guys."