Gerald Kooyman is a research professor at the Center
for Marine Biotechnology and Biomedicine at Scripps Institution of Oceanography.
Kooyman received his Ph.D. from the University of Arizona, where he studied
the diving behavior and physiology of Weddell seals in Antarctica. He is
the author of two books: Weddell Seal: Consurnmate Diver (Cambridge University
Press) and Diverse Divers: Behavior and Physiology (SpringerVerlag). Paul
Ponganis is an associate research physiologist at the Center for Marine
Biotechnology and Biomedicine, where he has collaborated with Kooytmn for
the past 14 years. He is also a practicing anesthesiologist in San Diego.
He received his Ph.D. from the University of California at Santa Cruz and
his M.D. from Stanford University. Address for Kooyman and Ponganis: Scholander
Hall, UCSD, La Jolla, CA 920930204. Internet: email@example.com; firstname.lastname@example.org.
People flatter themselves by placing humankind at
the top of the evolutionary tree. The implication, of course, is that people
represent the "paragon of animals," the perfect marriage of noble reason
and angelic form, to paraphrase William Shakespeare. Ironically, what people
do with this much lauded ingenuity is fashion devices that allow them to
mimic the animals. One of human kind's greatest achievements, after all,
is the invention of flying machines.
Some animal tricks still elude people. Take, for example,
deepsea diving. At present, the world record holder for a descent assisted
with weights and pulleys has reached a depth of 133 meters, a feat that
required the diver to hold his breath for longer than two minutes. Most
marine mammals can exceed that depth within their first few months of life.
And the premier divers in the animal kingdom elephant seals and sperm whales
occasionally dive to depths greater than a kilometer.
The restraints on people relate to their very basic
need for oxygen and their difficulty in dealing with dramatic changes in
pressure. Without the means to extract oxygen from the water, a diver must
take in all of the oxygen he or she will use for the duration of the dive
before becoming submerged. Further complicating matters is the way the
human body reacts to the increasingly high pressures encountered during
the descent. The pressure at depth becomes enormous, enough to collapse
the diver's lungs and force all remaining oxygen out of them.
But of all the dangers, the greatest are apparent
when the diver ascends toward the surface. On the way up, the decrease
in pressure poses a range of perils, including decompression sickness,
commonly known as "the bends," and "shallow water blackout," a probable
result of a sharp drop in the concentration of oxygen in the arteries,
ultimately reducing the amount of oxygen that gets to the brain. This in
turn causes the diver to lose consciousness just before reaching the surface.
Indeed, most human diving accidents occur on the way up, not down.
Curiously, marine mammals and birds do not seem to
experience these problems, although one would expect them to. The respiratory
systems of diving mammals are basically the same as ours. These animals
are dependent on their lungs for respiration just as people are. In spite
of these similarities, the deepsea divers among them can remain submerged
for long periods, up to two hours, and there is no indication that they
suffer from the bends on ascent.
Marine biologists have long wondered about the differences between the deepest sea divers and animals restricted to more shallow depths. Initially, their questions focused on the most superficial aspects of the dive: how far and how long? More recently biologists have developed the tools to ask more sophisticated questions. Our own research and that of our colleagues has shifted to is sues of the anatomical and physiological traits that allow these animals to do what no human being can ever achieve without mechanical devices. These studies so far indicate that the answer comes down to oxygen the way it is distributed to, stored by and consumed in the body's various tissues and organs.
Expert marine divers are found in every ocean from
the North Pole to the edges of the Antarctic continent. A couple of hundred
million years ago, reptiles dominated the seas with some of the most unusual
species of vertebrates that have ever existed. Now they are a remnant of
the past, with only one lizard, the Galapagos marine iguana, seven species
of sea turtles and about 50 species of sea snakes being adapted to draw
a reptilian living from the sea.
In our times, the greatest diversification and distribution
of sea-loving creatures (not counting the fish) is among endothermic birds
and mammals. Since they are able to generate and maintain their own body
heat, these two groups are not restricted to warm waters. In fact, they
have spread into temperate and even polar seas, where they are most abundant.
Among these polar creatures, the quintessential avian diver is the emperor
penguin, which can attain depths greater than 500 meters while staying
submerged for about 12 minutes. In shallower dives, an emperor penguin
may stay submerged even longer, over 20 minutes. Among mammals, the supreme
diver is the sperm whale, which can dive down over 2,000 meters, and the
northern elephant seal, which can descend to depths below 1,500 meters.
The Weddell seal, about which most is known and which we study, is somewhat
less dramatic in its dives. Still, it can descend to 700 meters, and at
times it may remain submerged for 82 minutes, which makes it far superior
Figure 2. Marine divers are
found in every ocean from the North Pole to the Antarctic and include mammals,
birds and reptiles. Initial research into these divers focused on the length
and depth of the dives. Such studies helped establish that the premier
divers were the sperm whale andnorthern
How is it that these animals,
which also have lungs, are so much better adapted than people to deepsea
diving? One glance at their bodies gives part of the answer. All of the
best divers are very streamlined, almost spindle shaped. The shape of the
penguin is so nearly resistance free that it has one of the lowest possible
drag coefficients. Diving mammals have little hair or very short hair,
and birds' feathers are modified in such a way that they glide nearly friction
free through the water. Aquatic animals have either shortened hind limbs
or none at all. And what would be forelimbs on terrestrial mammals are
modified to become flippers or fins. Aquatic birds use their wings as flippers.
Many of the most important adaptations have taken place internally and have to do with the way diving animals distribute and store oxygen. A universal modification within all deep divers, and perhaps the hallmark characteristic that sets them apart from all land forms, is the distribution and concentration of the protein myoglobin. Myoglobin is found primarily in muscle, and its main function is to bind oxygen. In some diving animals, particularly those that feed while submerged, the concentration of muscle myoglobin can be anywhere from 3 to 10 times that found in the muscles of terrestrial animals. This suggests that these animals store more oxygen in their muscles than do non divers and that, somehow, this relates to their ability to dive.
the bonds of glucose and storing that energy into the bonds of ATP is a
long and complex process. In effect, the glucose is burned very slowly
in steps that allow the formation of molecules of ATP at various points.
Nevertheless, the reaction does not proceed to completionunless
oxygen is present. In the absence of oxygen, only the very initial stages
of that process may take place. In this anaerobic phase of glucose metabolism,
only two molecules of ATP, are sformed
(versus 36 for each glucose molecule metabolized in the presence of oxygen),
and the end product is not C02 and water, but rather lactate. This accounts
for the buildup of lactate in the muscles of athletes who are exertingthemselves
beyond the rate of supply of oxygen. In this case, the muscles supplement
their aerobic respiration with anaerobic metabolism.
Since every cell in the body
requires energy and must therefore make ATP, every cell must get an ample
supply of oxygen. When people and animals breathe in air, they are taking
oxygen into their lungs, the first step in this distribution. Oxygen is
transferred from the lung to the blood, which contains the oxygen carrier
molecule hemoglobin. Hemoglobin carries oxygen to all tissues and organs.
In muscle, oxygen is transferred from hemoglobin to myoglobin.
3. Respiration, which generates energy from food, must continue even while
an animal is submerged. Inside cells, the bonds of the sugar glucose (C6Hl2O6)
the energy released is used to produce adenosine triphosphate (ATP). The
high energy bonds of ATP are more readily accessed by the cell than are
those of glucose and are used to power many of the cell's metabolic and
mechanical tasks. During glucose breakdown, the sugar's carbon and hydrogen
atoms eventually react with oxygen to form carbon dioxide (CO2) and water.
The complete oxidation of each glucose molecule generates 36 molecules
of ATP. In the absence of oxygen, glucose breakdown is incomplete, yielding
lactate in Place Of C02. The net yield of anaerobic metabolism is only
two molecules of ATP for each glucose molecule used.
relation between hemoglobin and myoglobin is an interesting one, since
the molecules are both functionally related and structurally similar. Myoglobin
is a protein in which sits a heme group, an organic structure that contains
iron. It is to the heme group, and specifically to the iron in the heme
group, that the oxygen binds. Hemoglobin contains four protein subunits,
each of which carries a heme group. As in myoglobin, the iron of hemoglobin's
heme group is the site of oxygen binding.Myoglobin
has a higher affinity for oxygen than does hemoglobin.When
blood passes through muscle, oxygen is transferred easily from the blood
to the muscle.
Most vertebrates that do not
have rich stores of oxygen in various tissues are extremely dependent on
having a supply delivered regularly to their tissues via the blood. People
fall into this category, and, as we know, we cannot go for very long without
breathing. But scientists started to wonder whether the same is true for
animals that can store oxygen in their tissues.
Figure 4. It is crucial that each organ and
cell receive sufficient quantities of oxygen. With each breath, an animal
takes in oxygen along with nitrogen and other gases in the air. In the
seal shown here, as in other animals, oxygen travels down the airway into
the lungs and there diffuses into the blood. Once in the blood, it binds
to the protein hemoglobin, which carries the oxygen to all of the tissues
and organs in the body. In muscle cells, the oxygen is transferred from
hemoglobin to a related oxygen carrying protein called myoglobin. The three
largest reservoirs for oxygen are the lungs, blood and muscles, and the
distribution of oxygen among these stores is important for diving animals.
Diving animals have 3 to 10 times more myoglobin in their muscles than
do their terrestrial counterparts, enabling divers to store more oxygen
in their muscles than do other animals. A potential consequence of this
is that the oxygen in the blood can be used by organs that do not store
oxygen, most notably the brain. Still other organs may practically cease
operation, so as not to use up oxygen. The abdomens of diving penguins
have been found to drop in temperature during a dive, suggesting a slowdown
in metabolic activity.
We would expect diving animals well endowed with muscle myoglobin to be less dependent for the duration of the dive on the blood to de liver oxygen. Rather, we think that during the dive, these deep-diving animals rely on the oxygen held by myoglobin. Other organs, notably the brain, do not store large amounts of oxygen. Flow is modulated as needed to other organs, depending on the nature of the dive. Our studies have aimed to measure oxygen uptake and the activity of various organs while animals are diving to see whether our predictions are correct. Investigators have also been measuring the blood flow to see whether, in fact, particular organs are preferentially serviced during a dive.
to its proximity to a re search station, the sound is an out standing study
site because it is over laid in early summer by a large plate of two meter
thick sea ice that has formed through the previous winter. Protected from
winds and currents, this 60 kilometer wide by 30 kilometer long sheet of
ice is wedged securely between Ross Island to the east and the Antarctic
continent to the west. At 77 degrees South latitude it takes until February
for the ravages of the sun to erode and weaken the ice enough for waves
and wind to fragment the sheet into floes that become part of the late
summer pack ice.
of the ice is particularly important since the two species we study the
Weddell seal and the emperor penguin both commonly dive under ice. We can
exploit both their diving habits and the ice sheet to prepare our study
site. We drill holes through the ice to introduce the diving animals. The
holes are placed at great distances from one another, making it unlikely
that an animal introduced into one hole will surface at another. This allows
us to measure sure accurately the length and depth of the dive by attached
recorders that are easily retrieved. We measure the time it takes the animal
to descend and ascend, the animals swim speed and how long the animal remains
at depth. We also look at the animal's heart rate, taking care to measure
how it changes through the course of the dive, which gives us some notion
of the circulatory patterns.
Figure 7. Magnitude and
distribution of oxygen in the various stores varies among species. For
each species shown here, the total oxygen store is given, as well as the
concentration typically held in each of the three stores.lungs, blood and
muscle. People maintain a lower supply of total body oxygen than do most
of the diving animals. In addition, the largest oxygen stores for people
are the lungs and blood, whereas the blood and muscle are the primary stores
in most diving animals.
want to know something about the animal's metabolism, we further prepare
the study site to allow us to measure oxygen concentrations. (So far, we
can do this only with the seals.) We place a plastic dome over the hole,
allowing us to measure the oxygen content within the dome before the animal
dives as well as after it has surfaced. By measuring the oxygen concentrations
within the dome while the seal is surfaced, we can make some calculations
about its metabolic rate and pulmonary function. We can also make some
calculations about the seal's oxygen capacity and usage.
distribution of oxygen in emperor penguins and Weddell seals implies that
oxygen is also used differently by the two during a dive. In seals, the
blood oxygen store dominates, and the lung oxygen store plays a minor role
in breath hold endurance. In penguins, lung oxygen stores are more important
than in seals, but the muscle oxygen store is the largest.
One of the
more difficult and contentious issues to come out of all this is whether
and when the diving animal exhausts its muscle oxygen stores. One would
expect that as an animal used up its store of oxygen it would be compelled
to switch from aerobic to anaerobic respiration. Since the end product
of anaerobic respiration is lactate, we would expect to see a rise in muscle
lactate with the increasing reliance on anaerobic metabolism. Previously,
investigators had reported seeing such a surge in blood levels of lactate
at the end of each laboratory experiment in which the animal was forcibly
sub merged, no matter how short the breath hold. Scientists interpret this
surge to mean that lactate is released into the blood from the muscles,
where it has been accumulating over the duration of the dive.
measured lactate levels in naturally diving Weddell seals, we saw something
quite different. We saw an increase in only about 5 percent of the dives,
and these were of the most extreme length. We have defined the time it
takes for an animal to express the rise in blood lactate as the "aerobic
diving limit," and are now trying to define the parameters that most contribute
to that limit. We think that the oxygen in each compartment is used at
different rates during a dive. Furthermore, we think that because the muscles
in diving animals contain so much myoglobin, it isless
important for blood to flow to muscle than it is for flow to be maintained
to organs that do not have an oxygen in store, most notably the brain.
But an animal has only so much oxygen in the an blood and muscle, and in
order to conserve these resources other activities must reduce their requirements.
We hope that by determining precisely how and where oxygen is being used,
we can find answers to such questions.
Figure 8. Since lactate
is a byproduct of anaerobic metabolism, the authors measure the time it
takes for lactate to appear in an animal's blood and have defined this
time as the 'aerobic diving limit.' In natural dives, the authors saw a
rise in blood lactate levels in only about 5 percent of Weddell seal dives,
and 21 percent of emperor penguin dives. They are now trying to define
the parameters that most con tribute to the aerobic diving limit.
laboratory studies on elephant seals by us and Antarctic field studies
of freely diving Weddell seals by Konrad Falke and his colleagues at Harvard
University have shown that blood nitrogen levels rise very little nomatter
how deep the dive. As noted ,before,
when the animals reach a relatively shallow depth of only 50 to 70 meters,
their lungs collapse and do not become reinflated until after the animal
ascends to shallow depth. This means that over the better part of the dive
the lungs are not functioning; they do not exchange gas, and much of the
nitrogen in the lungs never enters the blood supply. We presume that other
marine mammals experience similar lung collapse while at depth. Falke and
his colleagues have shown this to be the case in freely diving seals.
Figure 9. High concentrations
of nitrogen are hazardous to human divers. Nitrogen, which is a component
of air, passes into the blood as do oxygen and other gases. As the diver
rises toward the surface and the pressure de creases, the dissolved nitrogen
may form bubbles in the blood and other tissues, which results in joint
pain, neurological disorders and other complications. These effects, referred
to as the 'bends,' do not seem to trouble diving animals. Shown are data
taken during a WeddLI1 rL.1 dive, The concentration of arterial nitrogen
(top graph) reaches its peak long before the animal achieves maximum depth
(bottom graph). Nitrogen concentration then seems to decline to an equilibrium
between arterial and venous blood until the seal ascends.
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