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Squid studies: Escape and impairment

The views expressed are those of the author and are not necessarily those of Scientific American.


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san pedro mountain gulf of californiaEditor’s Note: Marine biologist William Gilly is on an expedition to study Humboldt squid on the University-National Oceanographic Laboratory System research vessel New Horizon in the Gulf of California. He and other scientists are learning about the giant squid, their biology and ecology on this National Science Foundation-funded expedition. This is his sixth blog post about the trip.

GULF OF CALIFORNIA—Days 10-13 Guaymas Basin: After a rousing night of steaming full speed into the wind, we awoke at dawn tucked in close to Isla San Pedro Martir, a tiny island that was high enough to protect us and several sailboats from the strong winds that were whipping up the Gulf. It can be an idyllic place—when it is calm, but when it is rough, there is little protection and it takes on a different character. Today was rough.

San Pedro Martir gulf of californiaSan Pedro Martir is home to many seabirds, mostly boobies that have deposited guano for centuries. In the right light, the little peaks look like they are covered with snow, but the tree-line of large cardons [cacti] suggests otherwise. If one examines the cliffs closely, you will see precarious rock cairns on the narrow ledges for storing guano. I do not know how old they are, but their primitive nature makes them look ancient. The island is now totally protected, so you will not see any more guano harvesters.

boobie in flight gulf of californiaDeep water of the Guaymas Basin, with a nice Oxygen Minimum Zone (OMZ), reaches this far north, and normally the deep basin to the west of the island harbors many sperm whales and big Humboldt squid. But radio reports we received a few days ago from whale researchers in this area indicated that there were no sperm whales this season—another strong suggestion of major ecological changes in association with the El Nino-like winter. But we wanted to come and check out San Pedro Martir for ourselves. Now that we are here, it is too windy to do much of anything. Rather than wait for calm weather, we decided to continue into the wind back to the middle of the Guaymas Basin. As we set out we are accompanied by boobies holding in the stiff breeze almost within reach.

Isla Tortuga gulf of californiaWe continue all day, and finally we can see a familiar landmark on the horizon, Isla Tortuga, the shell of a great turtle emerging from the sea. Perhaps it is the turtle that holds up the world. We will repeat our acoustic surveys, midwater trawls and jigging sessions in this area and then return to Santa Rosalia to fill in some gaps there. Although these data will make our work stronger, it seems in some ways like the denouement, and the attention of some of us turns again to shipboard experiments.

Brad Seibel’s group from the University of Rhode Island is studying not only small Humboldt squid in respirometry chambers, but also a variety of mesopelagic prey species that the squid consume, including other species of small squid. They are looking at respiration rates and at the level of anerobic metabolic products under hypoxic conditions. The goal is to elucidate the physiological and biochemical mechanisms used by Humboldt squid and their prey for coping with daytime life in the OMZ. Specimens are caught in the midwater trawls and quickly scooped out of the sample and placed in a dark cold-room until they can be used for experiments. It is difficult to get healthy specimens out of a large net, but slow tows help keep them in good shape.

squid in respiratory chamber for research in gulf of californiaMeanwhile, my team continues to examine escape behavior. It is challenging, and one major limitation has been the ability to reliably stimulate escape jets. We discuss ideas of visual stimuli, like a video image of a rapidly approaching object, or mechanical ones, like a quick jerk of the head. The latter idea came up because of a spot on the squid’s neck that we discovered was extremely sensitive to stimulation with mild electric pulses. What is more, the responses were extremely powerful and fast, hinting at a role for the giant axon system. And it turns out that there is probably a knob-like sensory organ right there that sends it output to the center of the brain that controls escape responses through the giant axon system. This is based on work on another species of squid, and some histology at home with some preserved specimens should determine if this so-called "neck-organ" is also present in Dosidicus. We would like to selectively stimulate this area in order to see how the giant axon system is used in escape responses. This is an extraordinary neural pathway for which the squid is justly famous.

Squid giant axons (single nerve fibers) have the largest diameter known. This makes them conduct rapidly, and the tremendous amount of branching of the final termination of these single-cell processes allows the entire mantle musculature to be thrown into a powerful all-or-none contraction whenever the giant axon fires. Both features are useful in an athletic behavior like an escape response. If we can get a handle on this system, it would provide a focused approach to the question of impairment of escape behavior by the cold, hypoxic conditions in the OMZ. Results so far are encouraging but hardly definitive. In one experiment, the fast, powerful responses triggered at the sensitive neck-spot reversibly disappeared when oxygen fell to a value about twice the level seen in the upper OMZ—and reappeared when oxygenated water was put back into the tank just above the threshold level. We crossed this threshold three or four times with the same results. In another experiment, the characteristic fast, powerful responses persisted to much lower oxygen levels, but other weaker components of the overall response, presumably not associated with the giant axon system, failed—this time irreversibly. So goes the early phases of any research in an unknown area. It is always a long slog, but the excitement at the beginning is intense.

But why would the squid’s escape response be impaired in the OMZ? Actually, it would seem impossible that such a highly athletic performance could not be impaired—who can run world-record marathons at the top of Mt. Everest? There is relatively more oxygen there than in the OMZ-home of the squid. I think the reason that sacrificed high-performance is acceptable is that everything else that lives at OMZ depths—and that the squid eats—is also slowed down. Large predators, at least fish like tunas, sharks and billfish, cannot spend much time hunting at such depths, because they tend to be limited by cold and low oxygen. A great deal of archival-tagging data shows that these pelagic predators hunt at relevant depths, but they cannot stay down very long. The Humboldt squid, on the other hand, is incredibly successful in this cold, hypoxic region—it can eat all day in a relatively safe environment. Perhaps impairment of the giant axon system at hypoxic depths is an acceptable compromise.

escape hatch sign on boat gulf of californiaThings get more interesting when you consider marine mammals, relative newcomers on the evolutionary scene. These deep-diving predators carry their own oxygen supply and maintain body temperatures far better than any fish—and they are reactive, intelligent and equipped with active-sonar echo-locating abilities for hunting in the dark. With the arrival of marine mammals, squids were dealt a new hand from the evolutionary deck, but I think they have not yet turned over all their cards. Give them another 10 million years, and they will do something clever.

You see a big radiation in cephalopod species diversity in the fossil record in parallel with the number of fish species—several hundred million years ago. Most of those cephalopod species (shelled ammonites and belemnites) are now extinct. But there was another great cephalopod radiation in parallel with the appearance and increasing diversity of marine mammals—tens of millions of years ago. Those species were the shell-less and highly mobile squid, cuttlefish and octopus. So there probably is an ongoing evolutionary struggle between squid and marine mammals, and the sacrifice of escape responses in Humboldt squid under OMZ conditions may be one of the things that need to be "corrected," at least from the squid’s point of view. I wish I could see how they end up doing it.

At the end of the day I am reminded about how difficult whole animal experiments are—because the animal controls the experiment. It was so much easier studying the dissected giant axon in isolation as a postdoctoral researcher in Woods Hole. Had I started my career at the organismal level, I probably would never have gotten very far. But the comfort of reductionism at some point must be sacrificed to develop a more holistic picture of how a certain protein or cellular element really works in the living animal—and how that animal functions in an ecosystem. Steinbeck says in the Sea of Cortez that we must to look from the tidepool to the stars and back again to achieve such understanding. He is right.

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