Mosquitoes use smell to see their hosts

On summer evenings, we try our best to avoid mosquito bites by dousing our skin with bug repellents and lighting citronella candles.

These efforts may keep the mosquitoes at bay for a while, but no solution is perfect because the pests have evolved to use a triple threat of visual, olfactory, and thermal cues to home in on their human targets, a new Caltech study suggests.

The study, published by researchers in the laboratory of Michael Dickinson, the Esther M. and Abe M. Zarem Professor of Bioengineering, appears in the July 17 online version of the journal Current Biology.

When an adult female mosquito needs a blood meal to feed her young, she searches for a host - often a human. Many insects, mosquitoes included, are attracted by the odour of the carbon dioxide (CO2) gas that humans and other animals naturally exhale.

However, mosquitoes can also pick up other cues that signal a human is nearby. They use their vision to spot a host and thermal sensory information to detect body heat.

But how do the mosquitoes combine this information to map out the path to their next meal?

To find out how and when the mosquitoes use each type of sensory information, the researchers released hungry, mated female mosquitoes into a wind tunnel in which different sensory cues could be independently controlled. In one set of experiments, a high-concentration CO2 plume was injected into the tunnel, mimicking the signal created by the breath of a human. In control experiments, the researchers introduced a plume consisting of background air with a low concentration of CO2. For each experiment, researchers released 20 mosquitoes into the wind tunnel and used video cameras and 3-D tracking software to follow their paths.

When a concentrated CO2 plume was present, the mosquitos followed it within the tunnel as expected, whereas they showed no interest in a control plume consisting of background air.

"In a previous experiment with fruit flies, we found that exposure to an attractive odor led the animals to be more attracted to visual features," says Floris van Breugel, a post-doctoral scholar in Dickinson's lab and first author of the study. "This was a new finding for flies, and we suspected that mosquitoes would exhibit a similar behaviour. That is, we predicted that when the mosquitoes were exposed to CO2, which is an indicator of a nearby host, they would also spend a lot of time hovering near high-contrast objects, such as a black object on a neutral background."

To test this hypothesis, van Breugel and his colleagues did the same CO2 plume experiment, but this time they provided a dark object on the floor of the wind tunnel. They found that in the presence of the carbon dioxide plumes, the mosquitoes were attracted to the dark high-contrast object. In the wind tunnel with no CO2 plume, the insects ignored the dark object entirely.

While it was no surprise to see the mosquitoes tracking a CO2 plume, "the new part that we found is that the CO2 plume increases the likelihood that they'll fly toward an object. This is particularly interesting because there's no CO2 down near that object - it's about 10 centimeters away," van Breugel says. "That means that they smell the CO2, then they leave the plume, and several seconds later they continue flying toward this little object. So you could think of it as a type of memory or lasting effect."

Next, the researchers wanted to see how a mosquito factors thermal information into its flight path. It is difficult to test, van Breugel says. "Obviously, we know that if you have an object in the presence of a CO2 plume - warm or cold - they will fly toward it because they see it," he says. "So we had to find a way to separate the visual attraction from the thermal attraction."

To do this, the researchers constructed two glass objects that were coated with a clear chemical substance that made it possible to heat them to any desired temperature. They heated one object to 37 degrees Celsius (approximately human body temperature) and allowed one to remain at room temperature, and then placed them on the floor of the wind tunnel with and without CO2 plumes, and observed mosquito behaviour.

They found that mosquitoes showed a preference for the warm object. But contrary to the mosquitoes' visual attraction to objects, the preference for warmth was not dependent on the presence of CO2.

"These experiments show that the attraction to a visual feature and the attraction to a warm object are separate. They are independent, and they don't have to happen in order, but they do often happen in this particular order because of the spatial arrangement of the stimuli: a mosquito can see a visual feature from much further away, so that happens first. Only when the mosquito gets closer does it detect an object's thermal signature," van Breugel says.

Information gathered from all of these experiments enabled the researchers to create a model of how the mosquito finds its host over different distances. They hypothesize that from 10 to 50 meters away, a mosquito smells a host's CO2 plume. As it flies closer - to within 5 to 15 meters - it begins to see the host. Then, guided by visual cues that draw it even closer, the mosquito can sense the host's body heat. This occurs at a distance of less than a meter.

"Understanding how brains combine information from different senses to make appropriate decisions is one of the central challenges in neuroscience," says Dickinson, the principal investigator of the study. "Our experiments suggest that female mosquitoes do this in a rather elegant way when searching for food. They only pay attention to visual features after they detect an odour that indicates the presence of a host nearby. This helps ensure that they don't waste their time investigating false targets like rocks and vegetation. Our next challenge is to uncover the circuits in the brain that allow an odor to so profoundly change the way they respond to a visual image."

The work provides researchers with exciting new information about insect behavior and may even help companies design better mosquito traps in the future. But it also paints a bleak picture for those hoping to avoid mosquito bites.

"Even if it were possible to hold one's breath indefinitely," the authors note toward the end of the paper, "another human breathing nearby, or several meters upwind, would create a CO2 plume that could lead mosquitoes close enough to you that they may lock on to your visual signature. The strongest defense is therefore to become invisible, or at least visually camouflaged. Even in this case, however, mosquitoes could still locate you by tracking the heat signature of your body . . . The independent and iterative nature of the sensory-motor reflexes renders mosquitoes' host seeking strategy annoyingly robust."

These results were published in a paper titled Mosquitoes use vision to associate odor plumes with thermal targets. In addition to Dickinson and van Breugel, the other authors are Jeff Riffell and Adrienne Fairhall from the University of Washington. The work was funded by a grant from the National Institutes of Health.