Fuel Economy of the White Shark
When a shark - or any other animal - eats a meal, it is consuming energy in the form of the chemical bonds that hold together atoms in stable arrangements called molecules. During digestion, these food molecules are disentangled, broken-down into smaller ones, and most are absorbed through the intestinal walls. The absorbed food molecules then pass into the bloodstream, which delivers them to the cells of the body. In the mitochondria of body cells, these food molecules are broken down, atom-by-atom, to release the energy contained in them. This energy can then be used to build new molecules (growth) or to drive the chemical reactions which characterize living things: muscle contraction (locomotion), active transport (osmoregulation, nerve cell function), manufacture of cellular secretions (hormones, neurotransmitters), and so forth. These various energy transformations are not 100 percent efficient, so that heat and locked-up energy (entropy) are inescapable by-products. In addition, metabolic reactions in all sharks (as in most animals) requires the presence of electron-greedy oxygen to sunder and dispose of used-up atoms, liberating carbon dioxide as an additional waste product.
The overall metabolic rate of animals can be estimated in a number of ways. For example, metabolic rate can be estimated by recording the amount of food absorbed - or better yet, its caloric value - over time, measuring the rate of weight loss in an un-fed animal, the amount of heat or oxygen given off, or the amount of oxygen consumed. In practice, measuring oxygen consumption is usually the method of choice when estimating the metabolic rate of fishes. To facilitate comparison of the metabolic rate for fishes of various sizes, oxygen consumption is usually expressed as the amount of gas consumed per unit of body mass. The most meaningful metabolic rate estimates are made on animals during well-defined activity periods. For fishes, the two best defined activity states are 'resting' - when the fish is quiescent and not under obvious stress - and 'active' - when the fish is forced to swim at its fastest sustainable rate. The resting metabolic rate of an animal is known as its Basal Metabolic Rate (BMR). BMR is usually the minimal rate of energy expenditure necessary to maintain life processes. When BMR for a given animal is subtracted from its 'active' rate, the difference represents the amount of energy it can direct toward greater levels of activity. This value is known as its 'scope for activity'. The BMR has been measured for a few inactive species of sharks and the active metabolic rate for a few small species that adapt well to aquarium tanks. But the White Shark is a large, active species that does not adapt well to the stresses of capture and containment. Until relatively recently, no one had opportunity to make measurements that could be used to estimate the overall metabolic rate of a free-swimming Great White.
In late June 1979, a dead Fin Whale (Balaenoptera physalus) appeared floating some 25 miles (40 kilometres) off Montauk Point, New York. Fifty feet (15 metres) long and in an advanced state of decomposition. The whale carcass created a pungent, oily slick many miles long. The slick attracted thousands of frenetically shrieking petrels, which repeatedly skimmed the water surface to feed on floating fat globules, and at least five White Sharks. Blue Sharks (Prionace glauca), which are ordinarily quite abundant off Montauk during summer and often gather in prodigious numbers at floating carcasses, were conspicuously absent. Perhaps buoyed by the gases liberated by decomposition, the whale carcass floated high - some 4.25 feet (1.3 metres) out of the water - and large, cavernous holes were clearly visible along the water-line, suggesting that the White Sharks had been feeding on the carcass itself. A fisherman harpooned a White Shark as it swam near the carcass; when examined by fisheries scientists, it measured 15 feet (4.6 metres) in length, 2,075 pounds (943 kilograms) in weight, and had 65 pounds (30 kilograms) of whale blubber in its stomach. Thus, the rotting whale carcass was definitely providing a rich banquet for attending White Sharks.
Word of this smelly feast soon reached Frank Carey and his colleagues, who quickly organized an expedition to study the White Sharks. Up to his untimely death in 1994, Carey was the pre-eminent investigator of endothermy in large pelagic fishes. It had long been suspected that the White Shark would eventually prove to be warm-bodied, like its close relatives. Carey had discovered and measured warm-bodiedness in the Shortfin Mako and Porbeagle back in 1966, and was very eager to demonstrate the same phenomenon in the White Shark. In anticipation of an opportunity to do so, Carey had prepared a thermistor 'harpoon' - sensor-equipped dart that could be plunged deep into a epaxial (upper back) muscle of a Great White and transmit the shark's location as well as simultaneous measurements of its swimming depth, body temperature, and surrounding water temperature. At long last, Carey had his chance.
Carey's experiment began on 1 July 1979. Chunks of meat were hung near the surface from the stern of a boat which was, in turn, tied to the whale carcass. A male White Shark, estimated to be 15 feet (4.6 metres) long, seized the bait and was struck with the thermistor dart as it turned away. The shark gave no reaction to being hit, circling around and taking a bite from the whale carcass. Over the next three-and-a-half days, Carey and his team tracked the shark, recording for the first time a Great White's swimming patterns and body temperature. Carey and his co-workers discovered that the swimming muscles of the White Shark are indeed warm, commonly 5.5 to 9° Fahrenheit (3 to 5° Celsius) above the water temperature. Because the red muscle of the White Shark lies in a band along the body cavity and close to the backbone, it is doubtful that Carey's team measured the maximum temperature of their specimen (later researchers have, in fact, measured White Shark body temperatures as much as 25° Fahrenheit [14° Celsius] above the ambient water temperature), but they were the first to demonstrate endothermy in this species.
The tagged White Shark's muscle temperature was not constant, however, but responded slowly to changes in water temperature. During the first 12 hours of the experiment, the water temperature registered by the thermistor decreased gradually, then sharply as the tagged shark made a series of dives into cold bottom water. These decreases in average water temperature resulted in a cooling of the shark's muscles. Changes in muscle temperature were slow and lagged behind changes in water temperature by several hours. The tagged White Shark thus did not appear to actively thermoregulate. Its muscle temperature changed slowly with water temperature and showed considerable thermal inertia. Since heat transfer by conduction is slow through such a large bulk of muscle, it is to be expected that muscle temperature would respond slowly to changes in water temperature. However, the results of Carey and his team's experiment strongly suggests that heat transfer from a White Shark's body to the surrounding water is greatly reduced by the rete mirable.
The White Shark tracked by Carey and his co-workers swam mostly within the well-defined thermocline (layer of water characterized by different temperature from that of water masses above or below it) that exists in the New York Bight area in summer. Depth telemetry indicated that the shark swam primarily between 30 and 60 feet (10 and 20 metres), in the cold water just above the upper surface of the thermocline. The fortuitous movement of the tagged White Shark from cold to warm water on 3 July allowed Carey and his co-workers to estimate its metabolic rate from the rate of change in its body temperature. At 21:00 hours, the thermistor indicated that the water temperature surrounding the shark increased abruptly from 58.5 to 62.1° Fahrenheit (14.7 to 16.7° Celsius). The thermistor indicated that, in response, the shark's muscle temperature increased from 64.5 to 68.0° Fahrenheit (18 to 20° Celsius) over a 17-hour period after entering the warmer water.
These temperature changes can be converted to metabolic rate as follows: if the animal were perfectly insulated, the production of metabolic heat would cause its temperature to rise; the rate of temperature increase would be directly related to metabolism. The shark, of course, was not perfectly insulated, and thus its body temperature was the result of an dynamic equilibrium between heat production and heat loss. When the tagged White Shark swam into warm water, this equilibrium was upset. But, with time, the temperature gradient was re-established at a new and higher temperature. Since the water was at all times cooler than the shark's swimming muscles, the net warming of its body was caused by metabolic heat production. By estimating the amount of heat needed to raise the Great White's body temperature at the rate recorded by the thermistor - adding a factor for metabolic heat lost through the gills and not appearing as a temperature rise - allowed Carey and his co-workers to estimate the shark's metabolic rate per kilogram (2.2 pounds) of body mass at 0.2 Calories (kilocalories) per hour. This is equivalent to an oxygen consumption of 60 milligrams per kilogram per hour.
In comparison with the White Shark, we humans are energy hogs. An average, healthy 20-year-old man has a BMR of about 0.97 Calories per kilogram per hour, or about 286 milligrams of oxygen per kilogram per hour. Merely sitting comfortably at room-temperature, a person uses nearly 5 times as much energy per unit of body mass as a Great White actively swimming in a cold ocean. But we humans are fully warm-blooded mammals, with our entire circulatory system maintained at a uniform 98.6° Fahrenheit (37° Celsius), even if the environmental temperature fluctuates by 72° Fahrenheit (40° Celsius) or more. Since its heart and gill circulation operate at environmental temperatures White Shark is only partially warm-blooded (hence my referring to it as 'warm-bodied' rather than 'warm-blooded'). It is therefore more meaningful to compare the Great White's metabolic rate with that of other sharks.
Metabolic rate measurements are available for a few species of sharks, mostly small individuals in warm water. Theoretically, a small shark would be expected to have relatively higher metabolic rates than a large one, and sharks in warmer environments to have a faster metabolic rate than those in cooler waters. If the metabolic rate for a Spiny Dogfish is scaled for size and temperature, it comes to about 20 milligrams of oxygen per kilogram of body weight per hour. Thus, a 15-foot (4.6-metre) White Shark has a metabolic rate only about three times that of a scaled-up dogfish - much less than the ten times one would predict based on body temperature alone. Thus the White Shark burns its fuel very efficiently.
Which raises an interesting question: how often does a large White Shark need to eat? Carey and his co-workers estimate that, with a metabolic rate of 0.2 Calories per kilogram per hour, 65 pounds (30 kilograms) of whale blubber would provide enough energy to maintain a 15-foot (4.6-metre), 2,075-pound (943-kilogram) White Shark about six weeks. Since the procedure used by Carey et alii would actually over-estimate the shark's metabolic rate, a large White Shark that had consumed a comparable quantity of caloric energy may be able to go two months or more between meals. At an average cruising speed of 2 miles (3.2 kilometres) per hour, a Great White may swim more than 2,900 miles (4,600 kilometres) on a single meal. No matter how an individual animal slices its total energy pie, that's terrific fuel economy!