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The Nose Knows: Sharks smell in stereo
[06.10.2010]
TAMPA, Fla. – When a lifeguard near Stuart Beach raced to rescue a screaming kite-boarder in February, he found the man – surrounded by circling sharks – had been mortally wounded. The shark-bite victim died as the lifeguard brought him to shore.

Shark attacks have been studied for years by researchers who hope to unlock mysteries around how the predatory animals use their senses. The answers may provide scientists with information that can help people – though in an unexpected way when it comes to the sense of smell.

Current Biology features an article by Jayne Gardiner, a Ph. D. candidate at the University of South Florida’s Department of Integrative Biology, and Jelle Atema from the Boston University Marine Program, on "The function of bilateral odor arrival time differences in olfactory orientation of sharks."

Basically, this means “sharks smell in stereo.”

Their research aims to “gain a better understanding of shark feeding behavior and of the concept of multisensory integration in general,” Gardiner said. Once understood, humans can benefit from what is learned.   

But first, figuring out how sharks use their noses requires special equipment and cooperative sharks. Gardiner fitted a headstage apparatus to a small, manageable species of shark known as the smooth dogfish. The equipment delivered controlled pulses of odor into the sharks’ left and right nostrils. 

“We carefully controlled the timing of the delivery of the odor and its concentration and found the sharks turn towards the side receiving the first, not the strongest, odor cue,” Gardiner said.  “This has implications for the evolution of the widened heads in the hammerhead shark family. These animals have more widely spaced nostrils than pointy-nosed sharks. When they swim into an odor patch at an angle, the wider spacing creates a longer time lag between the left and right nostrils, so hammerheads may be able to orient to odor patches at smaller angles of attack, potentially giving them better olfactory capabilities than pointy-nosed sharks.”

The way sharks track odor plumes and locate food has a correlation to how they respond to the timing of odor arrival.

“An odor plume is essentially a trail of patches of odor that are laid out by the water flow. The animal needs to successfully follow this trail to find food. We have found that there is a window of time lags, between 0.1 and 0.5 seconds that prompts turns toward the first side stimulated; if there is no delay or a long (one full second) delay, they turn left or right with equal frequency.”

There are reasons for and subtleties to how sharks turn from side to side as they swim through the water. Gardiner explained that “a brief delay in odor arrival between the nostrils tells the animal that it is encountering an odor patch at an angle and the brain tells the animal to turn towards the side receiving the odor first, i.e., to steer into the patch. If there is no delay, the brain says go left or right, you're hitting the patch head on. If the delay is long, the brain interprets it as two different patches and tells the animal to go either left or right. With each successive odor encounter, the animal makes another turn, so this ‘steering algorithm’ leads to the continuous side to side casting behavior and occasional circling behavior that we see as the animal tracks an odor plume to its source.” 

So far, this research does not have direct implications for interactions between sharks and humans, but there may be underwater navigation applications.

“The steering response of sharks has shown us a new, general principle that can be tested and perhaps implemented,” Gardiner said.  “Until our study, it was believed that aquatic animals locate odor sources by performing comparisons of odor concentrations at the two sensors (nostrils or antennae) and previous robots (for example, the robo-lobster) were programmed to track odors in this manner – and they failed. 

“With this new steering algorithm, we may be able to improve the design of these odor-guided robots, which may come in handy when looking for invisible chemical sources, such as explosives or the source of an oil spill or other chemical leak,” Gardiner said. “With the oil spill in the Gulf of Mexico, the main oil slick is huge and easily visible and the primary sources were easy to find, but there could be other, smaller sources of leaks that have yet to be discovered. An odor-guided robot would be an asset for these types of situations.”

Gardiner has spent literally thousands of hours observing sharks and working on various aspects of their behavior for a little over six years. She is a former student of Boston University's Atema, a biologist and an expert on how marine animals sense their environment. Their work has been featured on the Discovery Channel twice so far.

While the study in Current Biology looked only at sharks’ olfactory system, Gardiner also works on vision, the lateral line system, and the electrosense. Her research subjects include smooth dogfish, spiny dogfish, nurse sharks, bonnet head sharks, black tip sharks, and whale sharks. 

Originally from New Brunswick, Canada, Gardiner now lives in Sarasota, Fla. not too far away from the flume channel at the Mote Marine Laboratory where she conducts much of her research. A fascination with sharks was not what brought her to research them.

“Unlike most other shark scientists, I didn't enter into the field because of a life-long love of these animals,” she said. “I was however obsessed with fish and aquatic creatures in general and spent countless hours as a child catching frogs and fish at our lakefront cottage in New Brunswick. I used to keep them temporarily in a big Rubbermaid trash can to observe their behavior.”

In college Gardiner took a detour to study microbiology and immunology when people discouraged her from pursuing a career as a marine biologist. But the call of the sea was too strong.

“After a few years with the Canadian federal government, I abandoned a promising career to pursue my passion. After more than a year of discussions, Jelle (Atema) landed a grant from DARPA to work on shark sensory behavior and offered me a research assistantship. I thought, “well, a shark's a fish,” and the rest is history. 

“It took only a few weeks of working with these animals to realize how incredible their sensory capabilities are and just how little we know about them. I became particularly interested in understanding how these animals integrate the information from so many senses; in addition to the five senses that humans have, sharks also possess the electrosense.”

After earning a master’s degree from BU, Gardiner came to USF to work on her doctorate and expand the scope and scale of her research. Here she is co-advised by Philip Motta, an expert in feeding mechanics and Bob Hueter director of the Mote Marine Laboratory Center for Shark Research. They secured a collaborative NSF grant, with Atema and neurobiologist Allen Mensinger (University of Minnesota, Duluth) serving as co-PIs, to conduct a large-scale study on multisensory integration in four species of sharks. 

“These species each represent a different ecological niche - they hunt in different environments for different prey types, using different strategies to capture food,” Gardiner said. “We therefore expect that they will differ in the way that they rely on each of the senses for feeding. I am using sensory blocks to elucidate the complementary and alternating roles of the senses as the animals track, orient to, and capture live prey. In addition to looking at the larger scale movements and behavior of the animals, I am using high-speed to look at the very fine scale details of prey capture, looking for subtle changes in the way that the jaws move as a result of changes in sensory information used to line up the strike.”

Gardiner is concerned now about sharks survival.    

“Sharks have experienced a dramatic decline, some species have experienced a 90% reduction in numbers as compared to 20 years ago, and the more we understand these animals, the better we will be equipped to protect them.  Understanding how they use their senses to feed may help us develop better fishing gear, which may help reduce the numbers of sharks caught as by-catch.”

She points out that understanding sharks’ multisensory integration ultimately has implications for human health. 

“We know that people who have experienced a reduction or total loss of a particular sense often have heightened capabilities with their remaining senses as the brain undergoes a process known as somatosensory remapping. If we have a better understanding of sensory integration, we may be able to design adaptive devices that better bridge the gap between one sense and another, thereby improving the lives of those who have experienced sensory damage or loss.”

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Author: Barbara Melendez
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