Super-Charged Gills and Blood

We all know that people need oxygen to live, but few of us understand why. The reason has to do with chemical properties of oxygen itself. Oxygen has a remarkably high affinity for electrons, those tiny, negatively charged particles zipping around atomic nuclei in discrete orbitals. Oxygen is so 'greedy' for electrons because each atom is only two electrons short of having a full outer orbit, which is a lower, more stable energy state than remaining not-quite full. In order to become more stable, oxygen 'steals' outer orbital electrons from other atoms less able to hold onto them than itself. In living things, this electron theft occurs within tiny cellular organelles called mitochondria. The actual process is a complex cascade of electrons changing possession from one intermediate molecule to another and takes place on the highly folded internal membrane of mitochondria. At virtually every stage of this highly coordinated electron shuffle — which ultimately packages energy in the form of a chemical called ATP that is easily handled by living cells — oxygen, either acting alone or as part of other molecules, is the chief instigator. Essentially, the force with which oxygen rips away electrons from other atoms within mitochondria is what powers all multicellular life, including human beings and Great White Sharks.

The major function of the respiratory system of any animal is the exchange of oxygen and carbon dioxide (CO₂) between the environment and metabolizing cells. We humans and other terrestrial animals that breathe air inhabit a veritable ocean of oxygen: some 21% of the atmosphere is composed of oxygen gas (O₂, because, in the absence of other elements from which to steal electrons, an atom of oxygen will share with another of its kind). In contrast, aquatic animals — which need oxygen just as much as we do — must contend with much lower concentrations of this precious gas. Because the amount of dissolved gas a liquid can hold depends on its temperature, the ocean contains a maximum of about 4.5% oxygen in very cold water to a minimum of almost 0% in very warm water. Some aquatic animals reduce their total oxygen demand by remaining small or inactive or both. But a large, active marine animals like the White Shark must work hard to wrest enough oxygen from the sea to power its needs.

The first step is getting the oxygen-bearing medium to the actual site of gas exchange. Like many active sharks, the Great White relies largely on 'ram jet' ventilation — its own forward movement forcing water into the mouth, through the throat, and out the gill slits. But the White Shark may also employ a weak pumping action, contracting its pharyngeal (throat) and branchial (gill) muscles in a front-to-back sequence to help draw water into the mouth and squeeze it out the gills. This is the same rearward sequence of muscular contractions — albeit, performed rather more strongly — that allow certain bottom-dwelling sharks to lie on the substrate for extended periods. To the best of my knowledge, no one has observed a White Shark lying on the bottom, and this species relatively weak pharyngobranchial muscles may make it impossible to do so. Thus, the White Shark may be condemned to a life of perpetual motion, gasping for what little dissolved oxygen its gills can extract from the medium through which it swims.

As in other sharks, the Great White's gill filaments provide a relatively large surface for gas exchange. Of the White Shark's five gill arches, the first supports only a single row of gill filaments, while the remaining four support double rows. Each of the second through fifth gill arches supports a sheet of muscular and connective tissue (supported by cartilaginous gill rays) called a septum. Each septum — in turn — supports a row of gill filaments on either side, extending beyond them to form a flap over each gill slit. Some relatively inactive sharks and batoids (skates and rays) possess behind each eye an accessory respiratory organ called a spiracle, but this organ is minute or absent in the White Shark which relies exclusively on gill filaments to supply its respiratory needs. Along the top and bottom of each gill filament are delicate, closely-packed, transverse flaps of gill tissue known as secondary lamellae. It is these lamellae that are the actual sites of gas exchange in the Great White and other sharks. Each lamella is equipped with tiny arteries that carry blood in a direction opposite to that of the water flowing over them.

This counter-current flow brings oxygen-poor, carbon dioxide-laden blood in continual contact with fresh, carbon dioxide-poor, oxygen-rich seawater. Thus, the counter-current flow of blood and seawater maintains a steep concentration gradient, fostering the efficient diffusion of carbon dioxide out of the blood and oxygen in. When the blood holds an elevated concentration of carbon dioxide (diffused into the bloodstream as a waste product of cellular metabolism), it becomes slightly acidic and less able to hold onto the oxygen component of this gas, which then easily diffuses out of the blood at the gills. The blood's acidity thus reduced, oxygen can now diffuse from the seawater to the shark's blood via the gill filaments. To compensate for the relatively low concentration of dissolved oxygen in seawater, water passes over the secondary lamellae of sharks some 20 times more slowly than air remains in contact with the equivalent gas exchange sites (alveoli of the lungs) in humans. This delay allows sufficient time for dissolved oxygen to diffuse into a shark's blood.

Blood is a unique tissue in that it is largely liquid, composed of blood cells swept along in a viscous fluid called serum. As in humans, sharks have two basic types of blood cell, white and red. White blood cells are primarily involved in the body's immunological defense against foreign invaders (such as disease-causing microbes), while red blood cells are the main carriers of respiratory gases. In sharks, red blood cells are formed in the spleen (as they are in humans) and a peculiar structure in the esophagus called Leydig's organ (which is unique to elasmobranchs and seems to also play a role in the shark immune system). Unlike that of all non-mammalian vertebrates, shark red blood cells are nucleated and thus contain the genetic material DNA. (Pity there seems to be no undersea equivalent of a prehistoric blood-sucking insect preserved in amber, otherwise we could clone Megalodon and find out — once and for all — what this extinct mega-toothed shark looked like in life.) However, as in human blood, the primary oxygen and carbon-dioxide carrying molecule in shark blood is hemoglobin.

Sharks typically have larger and fewer red blood cells than teleosts, and thus must deal with longer average gas diffusion distances, making oxygen uptake at the gills less efficient. In order to compensate for this logistical hurdle, shark hemoglobin has a tremendous affinity for oxygen, becoming saturated at a partial pressure some 200% lower than that required by most teleosts. Perhaps most intriguing is the discovery that in certain egg-laying sharks, such as the Swell Shark (Cephaloscyllium ventriosum), fetal hemoglobin has a higher oxygen affinity than adult hemoglobin, possibly to allow for more efficient oxygen extraction from the relatively stagnant water within the egg case. A similarly enhanced oxygen-binding ability in fetal White Sharks may permit rapid growth in a womb that may be shared by as many as 11 oxygen-needy, carbon dioxide-venting pups.

Much of the detailed physiology of gas exchange in sharks has been worked out using small, captivity-tolerant species such as the Spiny Dogfish (Squalus acanthias), Lesser Spotted Catshark (Scyliorhinus canicula), and the Port Jackson Shark (Heterodontus portusjacksoni). Because oxygen's electron-stealing abilities are so important to powering multicellular creatures, evolution has conserved shark gas exchange mechanisms, retaining them with little or no modification. Yet the White Shark has evolved some fascinating respiratory adaptations that foster its actively predaceous lifestyle. An intriguing 1986 paper by physiological ecologist Scott Emery and pathologist Andrew Szczepanski studied gill dimensions in seven species of active, pelagic sharks including the Great White. They found that the White Shark has proportionately the longest gill filaments than any other species they examined. Long gill filaments substantially increase the total gill surface area per unit of body mass. For example, a 220-pound (100-kilogram) White shark has a total gill surface area of about 380 square feet (30 square metres), while a Blue Shark (Prionace glauca) of the same mass has a total gill surface area of about 150 square feet (14 square metres) — less than half as much. Emery and Szczepanski concluded that sharks with relatively large gill surface areas, like the Great White, increase the total amount of oxygen available to support their high energy lifestyle.

Blood Characteristics of the White Shark & Selected Other Creatures

Species	Hematocrit	Hemoglobin
White Shark Carcharodon carcharias	26 - 46	25 oz/pt (14 g/100ml)
Human Homo sapiens	38 - 42	25 oz/pt (14 g/100ml)
Bluefin Tuna Thunnus thynnus	41 - 52	3 - 3.6 oz/pt (15 - 20 g/100ml)
Blue Shark Prionace glauca	±28	1.4 oz/pt (8 g/100ml)
Spiny Dogfish Squalus acanthias	±19	0.7 oz/pt (4 g/100ml)

Yet another of the White Shark's adaptations to its high-energy lifestyle is found in its blood. Blood is composed of two basic types of tissue, cells and plasma. The percentage of blood volume that is composed of cells is called hematocrit. The hematocrit of a healthy adult man is about 42, while that of a healthy adult woman is about 38. In a 1985 paper, Scott Emery found that hematocrit of a White Shark ranges from roughly 26 to 46, averaging about 36. As the accompanying table shows, this value is high compared with other sharks and is on par with that of humans and Bluefin Tunas (Thunnus thynnus). In addition, Emery found that the amount of hemoglobin in a White Shark averages at least 2.5 ounces per pint (14 grams per 100 millilitres) of blood [one of his samples may have been contaminated with fluid from around the heart]. By comparison, a healthy adult woman has an average hemoglobin density of about 2.5 ounces per pint (14 grams per 100 millilitres) and a Bluefin about 3 to 3.6 ounces per pint (14 grams per 100 millilitres). Thus, the Great White has blood characteristics closer to that of humans and highly active teleosts than to most other sharks.