Moths are able to enjoy a pollinator's buffet of flowers – in spite of being among the insect world's picky eaters – because of two distinct "channels" in their brains, scientists at the University of Washington and the University of Arizona report.
One channel governs innate preferences of the palm-sized hawk moths that were studied. The moths can travel miles in a single night in search of favored blossoms such as southern Arizona’s sacred datura flowers. The moths key into the flowers’ scent.
When the moths’ first choice of flowers is not available, the other channel allows hungry moths to learn about alternate sources of nectar such as agave flowers. Being able to seek and remember alternate sources of food helps the insects survive.
The giant hawk moths known to scientists as Manduca sexta are innately attracted to flowers with a particular scent profile, said co-author John G. Hildebrand, Regents’ Professor and head of the UA department of neuroscience.
“But when the moths can’t find datura in the hottest early part of the summer, they go to agave flowers,” he said. “Everything about those flowers is different, but Manduca go to them and learn they can get a great nectar reward there.”
“This underscores the importance of learning in the feeding behavior of these animals,” he said. “People think about bees as insects that can learn, but not moths.”
A better understanding of the moth's neural basis of olfactory specialization and learning may lead to insights into how human noses and brains process odor, said Jeffrey Riffell, UW assistant professor of biology and the lead author on the research paper published Dec. 6 in Science Express, the early online edition of the journal Science.
Many of the mechanisms insects use to process olfactory information are similar to those of humans, he said.
The work builds on and extends previous research done by Riffell and several of his UA colleagues while Riffell was a postdoctoral researcher at the UA.
His co-authors on the current paper, “Neural basis of a pollinator’s buffet: olfactory specialization and learning in Manduca sexta,” are UA researchers Hong Lei, Leif Abrell and Hildebrand.
Manduca sexta moths, which have a wingspan of about four inches, are found in both North and South America and are important pollinators of night-blooming flowers. Their larvae, bright green caterpillars as thick as a man's thumb, are called tobacco hornworms. One alone can eat a tomato plant to the ground, Riffell said.
To investigate innate preferences, Riffell collected scent samples from flowers that hawk moths regularly visit in the wild. Scents also were collected from closely related flowers, some of which hawk moths tended to shun.
Abrell, an associate research scientist in the UA department of soil, water and environmental science and of chemistry and biochemistry, analyzed the scents in the lab.
The analyses showed most of the preferred flowers shared a remarkably similar chemical profile – one dominated by certain oxygenated aromatic compounds. Some are reminiscent of cherry soda or cotton candy, Riffell said.
It didn't matter that some of the preferred flowers evolved 10 million to 50 million years apart from each other – their scents have the same chemicals that attract hawk moths, Riffell said.
Moths smell with their antennae. To identify the olfactory channel that reacts when the moths were exposed to key chemicals from preferred flowers, Lei, an associate research scientist in the UA department of neuroscience, used electronics to record from sensory structures in the moths' antennae.
The moths’ olfactory systems responded the same way to the many different preferred flowers. Non-preferred flowers failed to activate the same neural pathways.
To check their findings, the researchers offered "naive" moths the scents of preferred and non-preferred flowers. Those moths had been raised on a soybean diet and had never been exposed to real flowers.
"What we found was really amazing. A naive moth will go mainly to flowers that had been attractive to moths in the wild, from flower to flower as if they were the same flower, responding in the very same manner," Riffell said. "These favored flowers look very different from each other. It's the odor that's driving the behavior."
Distinct from the channel that reacts to moths’ innate odor preferences, moths seem to use another channel when learning about alternate food sources, the scientists found.
In the wild, moths visit preferred flowers but also visit other flowers. The agave, or century plant, for example, is adapted for pollination by bats, but it is such a cornucopia of nectar that bees, birds and other pollinators seek out its flowers, Riffell said.
In the lab, the researchers trained moths to associate sugar-water rewards with the scent of agave flowers while recording their brain activity. The team found the chemical octopamine, an insect equivalent of norepinephrine, is released in moths’ brains as the signal to remember an important food resource.
Further, the scientists found learning about an alternate food source doesn't extinguish the moth's innate preferences -- something that can happen with bees. Together the two olfactory channels mean moths can survive in a changing floral environment, where at times their favored flowers might not be available, yet still maintain their innate preferences.
Using observations and experiments in both the wild and in the laboratory is an approach promoted by Hildebrand.
"This study is based on observations of wild animals in the real world. We think it’s critically important to know what the animals do in the natural world, not just what they do in the lab," said Hildebrand. "It's not enough for us to show what the animal can do under artificial conditions – we want to know the basis for what the animal does when it’s living out in the world."
Funding was provided by the National Science Foundation grants IOS 0822709 and CHE 0216226 and the National Institutes of Health grant R01-DC-02751.