Electronic tags broadcasting from the dorsal fins of salmon sharks reveal that these top predators migrate from the glacial waters of Alaska to the warm seas off Hawaii, according to a new study in the journal Science. The salmon shark's ability to survive such a broad range of thermal conditions is attributed to high levels of specialized proteins that keep its heart muscle cells beating at very low temperatures, say the study's authors.
"Sharks are declining globally, yet the movements and habitats of most species are unknown," says Stanford University biologist Barbara Block, chief scientist of the study, which included researchers from the National Marine Fisheries Service (NMFS), Monterey Bay Aquarium and the Alaska Department of Fish and Game. The research was conducted as part of the Census of Marine Life, an international network of scientists seeking to understand the abundance and diversity of life in the oceans.
Dual tagging technology
Writing in the Oct. 7 issue of Science, Block, Stanford doctoral student Kevin Weng and their colleagues compared the migration and unique cardiac physiology of the salmon shark—a close relative of the white shark—with the warmer, subtropical migration and physiology of the blue shark, another large predator.
In the study, the scientists used two kinds of satellite tagging technology. One, known as the Smart Position-Only Tag (SPOT), tracks individual sharks in real time as they migrate across the sea. The SPOT tag is attached to the tip of the dorsal fin, and when the shark surfaces, the exposed tag transmits the animal's position to orbiting satellites. Scientists can then download the data and follow the shark's day-to-day movements on their computers back home. In fact, this technology allows anyone with Internet access to track the sharks' daily migration in near-real time on a web browser: http://www.toppcensus.org.
"I like to check on the position of the sharks with my coffee every morning," says Block, the Charles and Elizabeth Prothro Professor in Marine Sciences at Stanford's Hopkins Marine Station.
The second technology, called the Pop-Up Satellite Archival Tag (PAT), records water pressure, temperature and light while the animal swims. Unlike SPOTs, which remain fastened to the fin, PATs detach from the animal on a pre-programmed date, then float to the surface and begin transmitting data to orbiting satellites. Combining the two technologies allowed Block and her colleagues to generate a rich dataset that included highly accurate details about each shark's position and diving behavior, as well as surrounding oceanographic conditions.
"We combined radio uplinking SPOTs that give us accurate positions and data-logging PATs that store information for the duration of the programmed mission," Block explains. "By using two types of tags, we're able to accumulate a larger dataset on the sharks' habitat and preferences with a greater accuracy than we've been able to do before."
To tag salmon sharks, Block and her colleagues traveled to Prince William Sound in the Gulf of Alaska during the summer. There, in calm fjords, they encountered acrobatic sharks leaping after pink, coho and other varieties of salmon returning to spawn. From 2002 to 2004, the scientists tagged 51 female salmon sharks. For comparison, co-author David Holts, a biologist with NMFS, led the researchers to the Southern California coast, where 31 blue sharks were outfitted with SPOT and PAT tags.
During the three-year study, the scientists obtained tracking data from 48 of the 51 salmon sharks. Twenty-one were double-tagged with SPOT and PAT instruments, while 27 carried one tag or the other. Six sharks were recaptured during the study, including three outfitted with pop-up tags containing full archival records of the sharks' minute-by-minute behavior. The longest distance traveled by an individual shark was 11,321 miles over 640 days—equivalent to traveling nearly halfway around the Earth.
All told, researchers collected more than 13,000 days of positional tracking data from the salmon sharks. "These data reveal a striking seasonal migration from subarctic to temperate and subtropical regions, presumably to forage or give birth to their young," says Weng, lead author of the study. In contrast, the satellite data showed that blue sharks remain in warmer Pacific waters off the continental United States and Mexico.
"The ability to follow many individuals for a year, and in some cases for two or more years, is virtually unprecedented," Weng notes.
To date, the researchers have used combined tagging on two other shark species, makos and common threshers. Block predicts that widespread use of this technique will provide much needed information about how sharks use the oceans. "From these data we can map areas of high use, visualize shark migration corridors and identify species-specific hot spots where shark populations may benefit from increased protection," she adds.
Warm bodies, cold hearts
The researchers also discovered that while some salmon sharks remain in the North Pacific for the entire year, others travel thousands of miles south to the subtropical waters of the Hawaiian Islands. During these long migrations, they encounter water temperatures ranging from 36 to 75 F (2 to 24 C). While in the cold subarctic, the sharks ranged between near-surface waters and depths as great as 450 feet.
"Sometimes in winter the surface waters, which are less salty, were so cold that the sharks spent more time in warmer, saltier waters below," Block notes. "When I glimpsed the sharks' radio positions from these frigid seas, I often wondered what it would be like to overwinter in the wilds of an Alaska fjord chasing herring in constant darkness."
As they move farther south, the sharks spend more time in deeper water, sometimes diving about a half-mile below sea level to avoid warmer temperatures at the surface.
The capacity to summer in the plankton-rich seas of the temperate north or to overwinter in chilly Alaskan waters sets salmon sharks apart from other laminids, a family that includes mako, white and porbeagle sharks. All laminids share the unusual ability of maintaining an internal body temperature that's up to 70 F warmer than the surrounding water. But the capacity to elevate internal body temperature does not extend to the heart, which is constantly flooded with blood that cools to ambient water temperatures as it passes through the gills to pick up oxygen.
As part of the Science study, the researchers sought to understand why the salmon shark's heart continues to function when it is ice cold. "The shark heart slows down in the cold, just as our own heart would," Block says. "But what sets it apart is where our heart would simply stop, the salmon shark keeps on ticking."
Laboratory analysis of heart tissue from six salmon sharks revealed high levels of specialized proteins that control the release and uptake of calcium ions, which are responsible for maintaining rhythmic cardiac contractions. The researchers discovered that the rate of calcium uptake by these proteins was about 10 times faster in salmon shark hearts than in blue sharks, which inhabit much warmer water. This finding may explain the ability of salmon sharks to maintain their heartbeat and supply their warm, active bodies with blood even as the heart cools to 35 F.
"This is clearly a unique shark species—the warmest of all gill-breathers in the ocean," Block observes.
The salmon shark project is part of the Tagging of Pacific Pelagics (TOPP) initiative, a research program affiliated with the Census of Marine Life. TOPP scientists use electronic tags to study the migrations of 22 species of marine animals throughout the North Pacific.
"Many sharks are threatened by fishing around the world, and biological knowledge is urgently needed to design management strategies," the authors wrote. "Satellite tracking technologies can be used to rapidly map shark habitats worldwide, which is critical to their future protection."
Other co-authors of the Science study are Stanford physiologists Pedro Castilho, Jeffery Morrissette and Ana Landiera-Fernandez; Robert Schallert, a technician at the Monterey Bay Aquarium; and shark biologist Kenneth Goldman of the Alaska Department of Fish and Game. The study was funded by the Office of Naval Research, the National Science Foundation and the Gordon and Betty Moore, David and Lucile Packard, and Alfred P. Sloan foundations.
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