Thoroughly Modern Migrants

Moths and butterflies—round-trip tickets not necessary

Hugh Dingle is gracious about geese and robins. They may be the most popular icons of migration, winging south in the fall and lifting people’s spirits in spring, when they finally honk or bob-bob-bob their way back to the same territory. For decades, a bird-based idea of migration dominated popular and scientific thinking: Individual animals went somewhere each year, then came back.

ROYAL JOURNEYS. Monarchs get called North America’s only migrating butterfly but scientists suspect other species migrate also. PhotoDisc

WATCH THIS SPACE. The red admiral, a seasonal migrant in Europe, may be following warm weather in the United States too. T. Lorenzin

HERE, THERE, EVERYWHERE. A relative of the red admiral, the American lady, is attracting attention of butterfly spotters who suspect that the species migrates. A. Lorenzin

In the 1960s, however, entomologists began to free themselves from the traditions of bird behavior and consider migration in broader terms, says entomologist Dingle of University of Queensland in Brisbane, Australia. Today’s view puts more emphasis on the behavior of the organism and less on the route.

An individual migrant, such as a monarch butterfly, doesn’t have to make round-trips. It can leave the return to future generations. But the migrant does have to behave in distinct ways. It ignores a lot of interesting stimuli, even neglects some of the normal chores of living. Depending on the species, the migrant may shun sex or food as it just keeps on traveling. It can’t act like a vacationer, open to new experiences on its journey.

This broader definition of migration, embracing the habits of certain moths and butterflies, has raised some old questions in new ways. Weather has always mattered in migration studies, but entomologists are now working to understand movements of air masses over continents to predict arrivals of hitchhiking populations of moths, including some of the most vexing of agricultural pests. Butterflies are being taken up as model organisms for studying navigation, and that research is moving to the molecular level.

No distractions

Butterflies have set the standard for fluttering around, foraging with plenty of zigzags and detours. So, a butterfly that keeps a fairly consistent heading, especially when flying more than 8 feet off the ground, is a suspected migrant.

This relatively straight movement counts as one of the five typical signs of migratory behavior, says Dingle, who has relied on his own findings and the data of others to write extensively on migration. Another migratory characteristic is unusually prolonged travel.

Suppression of some normal appetites is another item on Dingle’s list. The migrating butterfly, for example, might flap over patches of otherwise-enticing flowers.

Migrants also typically have distinct behaviors for starting and stopping their journeys. As the final sign of migration, they often reallocate their assets before the trip. A monarch butterfly, under good conditions, can store up to 125 percent of its lean, dry weight as fat. Also, a monarch going south in the fall stays in a stage of arrested sexual development.

Those characteristics show up not only in recognized migrators but also across a broad range of species. In Dingle’s 1996 overview, Migration: The Biology of Life on the Move (Oxford University Press), he extended the term migrant to seeds hitchhiking in an animal’s gut and fungal spores wafting on the breeze.

Just how many moths and butterflies fit this definition remains an active area of research. One thing entomologists will say for certain is that some of a farmer’s least favorite moths migrate.

Blowing in the wind

The first inkling of a windblown distribution of migrants in northern North America came from farmers who had linked certain pest outbreaks with winds from the south. Later, in the 1920s and 1930s, when planes captured high-altitude air samples, scientists routinely found insects, spiders, and mites 1.5 kilometers off the ground. As radar and wide-scale weather monitoring improved, researchers figured out that many teensy animals fly high into the atmosphere and catch the wind for a long, fast ride.

One agricultural pest, the fall armyworm moth, blows from the south to the northeastern and north-central United States and bursts out in abundant populations in the new territory, according to Dingle. Many of these moths die there, but fall weather patterns let enough offspring escape to head back to the warm south to perpetuate the species.

Scientists called radar entomologists, working with meteorologists, have developed several types of radars for detecting incoming masses of insects, such as the corn earworm moth. Similar airborne migrants bedevil farmers in Asia, Africa, and Australia. The radar entomologists are examining how the weather affects the migration patterns.

“High-altitude migration is very common, probably much more prevalent than the more-visible daytime migration of butterflies at low altitude,” says Alistair Drake of the University of New South Wales in Canberra, Australia. Drake points out that in much of the world, such as temperate North America, weather patterns change seasonally, so an insect population can often catch a ride on the wind for both parts of the round-trip.

Entomologists have argued that only a round-trip journey for the population makes evolutionary sense in climates where it can’t live year-round. Otherwise, the genetic drives for migratory behavior would just be taking a one-way ride out of the gene pool.

Flutter power

Though butterflies and moths aren’t exactly hunks of rippling muscle, some add their own power when riding on the wind. Robert Srygley of the Smithsonian Tropical Research Institute in Panama studies migration in tropical butterflies.

Several species of sulfur butterflies, for example, fly southwest across Panama after the rainy season begins. They may not be noticeable to the untutored eye on their journey inland, but when they cross open water, “it’s a river of butterflies,” says Srygley. “They were bright yellow against a gray thunderhead in the sky,” he remembers of one of his more spectacular sightings.

Another of these yellow migrants, the cloudless sulfur butterfly, Phoebis sennae, flaps its way over the Caribbean Sea in December. Srygley and his colleagues have followed along in boats, monitoring the migrants’ direction and speed.

In 2001, the team reported that males and females respond differently to wind. Males keep flapping even when they catch a good tailwind that carries them along, presumably putting more energy into the flight. It’s as if they need to reach their destination as soon as possible. Females of the same species instead let the wind do most of the work.

Srygley contends that the strategies make sense, considering the differing pressures on the sexes. For a male, flapping into the breeding grounds early means extra opportunities to mate. In contrast, what probably matters to a female is arriving with enough fat reserves to produce abundant, healthy eggs. Thus, a less demanding flight makes sense for them.

For many other butterfly and moth species, observers are still working on the basics of who flies where when. Since many of these species don’t bother crops, and therefore don’t attract agricultural funding, monitoring falls to volunteers.

“I hear people say that the monarchs are North America’s only migratory butterfly,” says Royce Bitzer of Iowa State University in Ames. “And I say, ‘Well, we don’t know that.'”

Bitzer is putting together an Internet site where people can report sightings of several Vanessa butterflies, such as painted ladies and red admirals, that he suspects of being migratory (http://www.public.iastate.edu/~mariposa/homepage.html). In his informal network, he’s collected some 80 sightings per year for the past 4 years. Every few years, such as in 2003, a great mass of painted ladies erupts in Western towns and seems to move in a northeasterly direction. Bitzer, however, suspects that in other years, a smaller group of these butterflies works its way north in the spring and south again in the fall.

Bitzer’s site has company. The United Kingdom, for example, has a moth-spotting network, and Finland has a Web site where people can report sightings of moths and butterflies.

“The Netherlands may be a small country, but we have the longest ongoing registration of migrating lepidoptera in the world,” says Rob de Vos of the Zoological Museum of Amsterdam. Today, his network of about 240 volunteers depends on the Web, but the project started in 1940. Each year, the spotters log 20 to 30 species of what de Vos calls “real migrating lepidoptera,” which can’t hibernate in the Netherlands.

Royalty

The biggest U.S. Web collections of sightings focus on North America’s favorite migrating butterfly, the monarch. (For example, track this year’s monarchs at http://www.learner.org/jnorth/.)

Biologists have already worked out the basics of monarch migration. In the eastern and midwestern United States, the populations of monarchs fly in the fall to specific overwintering havens, mostly in the fir forests of central Mexico.

Canadian monarchs fly down there too, says biologist and glider pilot David Gibo of the University of Toronto at Mississauga. For them, the trip covers 4,500 km. That’s about 150 million body lengths for the monarch, Gibo points out. To match that feat, a 6-foot-tall person would have to travel 270,000 km, or about 11 times around Earth.

Butterflies that survive the trip spend the winter in a hormonal state that suppresses mating. When spring comes, these butterflies, which have lived much longer than their parents, start the trip back. They make it only as far north as the Gulf Coast, where they reproduce in the first flush of milkweed growth of the new year. It’s the next generation, and the next, and the next, that finally make it all the way the back to their ancestors’ starting points in the United States and Canada.

The generation that flies south and overwinters lives about 8 months, whereas the other generations survive only about 6 weeks.

West Coast monarchs winter on the California coast at spots from just north of San Francisco to northern Baja California. Or at least that’s what the prevailing opinion has been. Dingle says that he and his colleagues are analyzing the collection date and location of monarch museum specimens from the West. The team is beginning to suspect that a good portion of these butterflies fly to Mexico, as the populations further east do.

The monarch is the only butterfly known to return to small, specific areas for overwintering. So, scientists have wondered just how butterflies scattered across the North American continent could find their way to, say, the same handful of forested hillsides in Mexico that their ancestors left at least two generations before.

It appears that they rely on several guides. Some 50 years ago, biologists discovered that both honeybees and starlings use the sun in navigating, so monarch biologists speculated that butterflies, too, might find some kind of sun compass in their subjects. Tests in the late 1990s looked promising.

More recently, Henrik Mouritsen and Barrie J. Frost of Queen’s University in Kingston, Ontario, developed a new kind of flight simulator, in which butterflies fly much longer in controlled tests than they had in previous ones. The simulator blows air from a computer fan at tethered butterflies and measures their orientation with a customized component from a computer mouse.

In 2002, the researchers published results from tests in which butterflies kept under various light-dark cycles were permitted to fly in the simulator under natural sunlight. If an animal used the sun for orientation, a theory went, the animal must have a built-in clock to compensate for the sun’s daily arc across the sky.

Monarchs in Ontario generally fly southwest as they start their migrations. However, when the researchers artificially advanced daylight by 6 hours and then put these butterflies into simulators, the monarchs oriented as if the morning sun were already in the west instead of still rising in the east. Butterflies that had adapted to a delayed daylight regimen did the opposite.

Such mistakes, the researchers concluded, indicate that the monarchs indeed use a sun compass.

Work published in the May 23, 2003 Science has started to reveal the molecular innards of the clock. “My interest is in circadian rhythms,” says neurobiologist Steven M. Reppert of the University of Massachusetts Medical School in Worcester. The travels of other timekeeping navigators that neurobiologists could study, such as honeybees and desert ants, might involve learning and memory. But a monarch heading for its overwintering site has never been there before. “The nice thing about the monarch butterfly is that you’re dealing with an animal that’s pure genetic instinct,” says Reppert.

The first step in this research project was to “take a sledgehammer and see what happens when you break the clock,” says Reppert. That sledgehammer turned out to be constant light. Reppert, Oren Froy of the University of Massachusetts, and their colleagues reported in the Science paper that when butterflies from a constant-light regimen flew in the simulator, they navigated dreadfully, flying toward the sun without correcting for the time of day.

The researchers began to link the disruption of the compass to genes by sledgehammering another time-related process: the roughly synchronized emergence of adults from their pupal stage. Constant light disrupted the timing of this too, and for this process, the researchers showed that out-of-whack insects had out-of-whack activity in a specific gene. In fruit flies, that gene, per, is a major cog in the circadian clock.

Monarchs, like some other insects, seem to use the polarization of light in their orientation, Reppert and his colleagues reported in the Jan. 20 Current Biology. As sunlight blasts Earth, the atmosphere distorts the light, and a creature with the right kind of eyes can see a pattern of polarized light that can aid in orientation. When researchers covered the flight simulator with a filter that twisted the polarization 90 degrees, the butterflies predictably went off course.

Scientists have found magnetic-compass navigation in a wide range of creatures. These include some migrators—salmon, tuna, some birds—and also bacteria, amphipod sandhoppers, newts, and the American alligator.

Magnetic compass navigation hasn’t yet been shown in butterflies. An experiment in 1999 seemed to demonstrate that migrating monarchs responded to the magnetic field, but in 2000, the researchers withdrew the paper. The results had been skewed by the butterflies’ reactions to the observers’ clothes, said the withdrawal notice.

The 2002 experiments in Ontario found no evidence of any magnetic-compass effects, but Srygley is still looking for a butterfly’s magnetic sense.

Tricky as the problems of migration are, they continue to attract popular and scientific curiosity. Dingle said it best in his book: “For sheer drama and beauty, it is hard to match the movements of millions of individuals over what are often sizable portions of the surface of our planet.”

Susan Milius

Susan Milius is the life sciences writer, covering organismal biology and evolution, and has a special passion for plants, fungi and invertebrates. She studied biology and English literature.

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