The spitting image: Mouse eats fruit while plant controls mouse!

Animals use plants for food, shelter and medicine. But plants also use animals for pollination and spreading seeds.

In the course of evolution, plants and animals change their structure, behavior and chemistry to survive and get what they need from the other side. Now we hear of a mouse from the Negev Desert in Israel that eats watery berries of a desert shrub called Ochradenus baccatus, but spits out the high-protein seeds.

The curious behavior is a result of the plant’s ceaseless struggle to survive and reproduce.

The common spiny mouse seems to know that eating the seeds will start a reaction creating a super-toxic brew, called a “mustard-oil bomb” because it contains a chemical that adds zip to mustard. Since the reaction cannot start until the seeds are opened and exposed to an enzyme in the pulp, a mouse that lets the seeds dribble from its mouth while eating the pulp can skip the mouthful of Yuk! and still savor an organic fruit drink.

How choosy are these mice? When the experimenters fed them fruits without the enzyme, they ate the seeds – proving that the response was not hard-wired into their brains.

“We started this study believing that rodents would be a good model for studying the effect of defensive chemicals in ripe fruits on seed predators,” first author Michal Samuni-Blank told us via email. “It was very unexpected to find out that for our model plant, this rodent is a very efficient seed disperser.”

The mice have good reason to spit, adds Samuni-Blank, a biology Ph.D. candidate at the Technion in Israel. “The fruit itself can be quite sweet. However, I can feel the bitterness when I taste the mashed fruits (pulp and seeds). Sometimes it is very disgusting and the bad flavor can stay for quite a while… Ugh!!!”

A sweet and sour fruit

Taily weed is grazed by camels, rodents, lizards and birds. “Most animals in the desert are in desperate need of water,” so any desert plant that makes fleshy, watery fruits needs a good defense, says co-author Denise Dearing, a professor of biology at the University of Utah.

To get animals to distribute its seeds, the plant has evolved a two-part flavor “bomb” that only explodes when damaged seeds contact the pulp, Dearing says. “The fruit has a precursor to the toxin and the seed has the activator [an enzyme], so when the seed is crushed, the pulp becomes toxic.”

This study is “the first reported evidence of seed dispersal via seed spitting by rodents,” says Samuni-Blank. “Our results demonstrate, for the first time, the conversion of a rodent from a seed predator to a seed disperser.”

Rapid rodent transport

The mouse gets a fruity snack without the toxic aftertaste, but the mouse also transfers the plant’s seeds to new locations.

Samuni-Blank was the first to notice the subtle expulsion of the seeds while the mice were eating dinner, Dearing notes. “It does not spit them out like we spit a watermelon seed across the room. Somehow they manipulate the very tiny seeds from the pulp and let them dribble down the side of the mouth.”

This discovery, Dearing says, “raised the issue that this seed predator did not seem to be a seed predator all the time.” The dispersal seems efficient: for unknown reasons, mouse-spat seeds germinated twice as well as bird-excreted seeds.

A seed in need is no feed indeed!

Although animals are often categorized as seed eaters (including many mammals) or seed dispersers (including many birds), the study shows a single species switching roles according to the situation.

But the “mustard-oil bomb” is a powerful educational tool: a mouthful of nasty persuades the mouse to think twice before eating those seeds again.

Revolution in evolution?

Yet when Samuni-Blank raised mice in captivity, “she found that if she deactivated the enzyme in the seed, they would eat the seeds along with pulp,” says William Karasov, an expert in physiology and evolution at the University of Wisconsin-Madison.

That’s exactly the opposite to what occurs in nature, where the enzyme is present.

Two-part toxins have been known for many years, says Karasov, a co-author who studies digestive physiology and evolution. “The new part is that the plant’s toxin portfolio is manipulating the behavior of this animal.”

“Most examples of this kind of plant defense involve animals that have fixed behavioral or physiological responses,” Karasov adds. “This shows a lot of real-time adaptability on the part of rodents.”

“In the coevolutionary arms race between plants and animals, at first glance, it seems as if the mouse is winning, as it has circumvented the toxin that the plant has put there,” says Dearing, an expert in animal responses to plant toxins.

But the outcome is “a much more complicated story than we started with,” Dearing adds. “Both sides are winning; the mouse gets pulp that’s free of the toxin, and the plant’s seeds get spread.”