Butterflies and bad taste: rethinking a classic tale of mimicry - viceroy butterfly not a mimic of the monarch butterfly

Science News, June 1, 1991 by Tim Walker

Picture a bird searching for a mid-afternoon snack -- perhaps a butterfly. After all, butterflies fluttering from flower to flower make easy targets for a swooping bird.

Suddenly, the bird spies a bright orange butterfly. But instead of attacking, the bird ignores it. Why? Because the bird remembers what happened the last time it ate a bright orange butterfly: It vomited.

So the butterfly survives and continues on its way, courtesy of the bright orange warning that nature painted on its wings.

But was this a false warning? Did the butterfly's color trick the bird into passing up what would have actually made a tasty hors d'oeuvre? If the orange butterfly was a viceroy, Limenitis archippus, most biologists would have answered yes. For more than a centruy, the conventional wisdom has held that this winged insect cloaks a very appetizing body behind the colors of a toxic monarch butterfly, Danaous plexippus.

New research indicates, however, that the viceroy has successfully deceived scientists, not birds. Entomologists have long labored under the assumption that the viceroy's orange warning colors were just a bluff. Now, two zoologists have demonstrated that to discerning birds, the viceroy can taste just as foul as the noxious monarch.

Nineteenth-century English naturalist Henry Walter Bates first put forth the idea that a species of taste butterfly could protect itself by evolving to mimic a toxic species. He based this hypothesis on his observations of butterflies in the Amazon river basin during the mid-1800s. One species' exploitation of another's protection system has been called Batesian mimicry ever since.

And for most of this century, biology textbooks have touted the viceroy-monarch relationship as the classic example of Batesian mimicry -- a truism that must now be reconsidered.

David B. Ritland and Lincoln P. Brower of the University of Florida in Gainvesville have conducted an avian taste test, serving up the addomens of seven different butterfly species, including viceroys and monarchs, to local red-winged black-birds. The test aimed to determine which butterfly species, if any, were noxious to the birds. Because these snacks lacked wings, the birds had to base their selections on the taste of the butterflies' bodies alone.

The birds found the viceroy just as unappetizing as the monarch, the zoologists report in the April 11 NATURE. In fact, the birds rejected more than one-third of the viceroy bodies after pecking them just once. These results "clearly refute the traditional hypothesis that viceroys are palatable Batesian mimics," Ritland and Brower say.

Butterfly mimicry is more than a curious biological sideshow. Deciphering mimicry relationships helps biologists understand some of the complicated and dynamic forces that affect the evolution of a species, Brower says.

Why had no one challenged the viceroy's avian palatability before?

One reason, says entomologist Austin P. Platt of the University of Maryland-Baltimore County in Catonsville, is that the viceroy evolved from a group of tasty admiral butterflies. "So it was just widely held that the viceroy itself was also palatable," he explains.

During the last several years, however, a few experiments began to cast doubt on the viceroy's supposed tastiness, according to Richard I. Vane-Wright of the Natural History Museum in London, England. But those experiments used whole butterflies, Ritland says, which meant that the taste-testing birds could have rejected the viceroys because of their orange wings and not because of any noxious taste.

Moreover, Vane-Wright says, many biologists believed butterflies couldn't manufacture their own toxic chemicals to defend themselves from predators; instead, from predators; instead, the insects had to absorb the toxins of poisonous plants during their caterpillar stage. And viceroy larvae don't feed on toxic plants.

The adult monarch's chemical defense, however, does depend on toxins in the milkweed plants on which its caterpillars feed, Brower notes. Because monarch caterpillars incorporate the heart toxins, called cardiac glycosides, that milkweeds rely on for their own defense against herbivores, eating a monarch can "really set a bird's heart jumping," he observes.

But the toxicity of an individual monarch depends on the variety of milkweed it ate as a caterpillar, Brower says. A bird that eats a monarch butterfly that dined as a caterpillar on a mildly toxic variety of milkweed will not be poisoned. But a monarch caterpillar feeding on a strongly toxic milkweed variety will become a truly toxic butterfly, potentially deadly to any bird that eats one and doesn't vomit it back up.

Viceroy caterpillars, in contrast, feed on nontoxic willows, and this suggests that viceroy butterlies somehow manufacture their own chemical defense, Vane-Wright says. The observation supports a new view among some lepidopterists that not all butterflies depend on plant poisons for their defenses, but instead develop as "masters of their own evolutionary fate," he says.