Circulation and a Wonderful Net
Right now you are burning. Your body is busily oxidizing your last meal, converting it into new tissue, energy, and heat. This internal combustion is a 'slow burn', but the result is the same as a roaring bonfire: carbon compounds are combined with oxygen, breaking them down and producing thermal energy in the process. The greater the difference between the temperature inside and outside your body, the more rapidly you radiate this heat to the environment.
The body temperature of most creatures — including insects, fishes, and reptiles — fluctuates with the temperature of their environment. This is known as 'ectothermy' or 'cold-bloodedness'. Because they cannot maintain a constant body temperature, cold-blooded creatures tend to live where the average environmental temperature is optimal for them. But birds and mammals are able to physiologically regulate their internal temperature within a narrow, optimal range. This is called 'endothermy' or 'warm-bloodedness'. Our warm-bloodedness has (in part) enabled our species to extend its range from the warm equatorial tropics where we evolved to the cold temperate zones of higher latitudes. In cold environments, we can use insulation to help maintain our bodies' internal temperatures.
Water conducts heat many times faster than air, draining precious body heat with relentless efficiency. When diving in cold water, we humans rely on dry or wet suits to insulate us against heat loss by trapping a layer of warm air or water against the skin. If humans venture into a cold aquatic environment without such insulation, our internal thermostats need to work overtime to prevent hypothermia. I'm sure you will agree it is much easier (and more comfortable!) to swim in warm water than to warm cold water with your body heat. Many types of marine animal — including most sharks — are ectothermic, and thus are most abundant in warm waters. But studies by Frank Carey, his co-workers and colleagues have revealed that at least seven species of lamnoid sharks — the Great White, the Longfin (Isurus paucus) and Shortfin Makos, the Porbeagle (Lamna nasus) and Salmon Shark (Lamna ditropis), the Common (Alopias vulpinus) and Bigeye (Alopias superciliosus) Thresher — have successfully invaded cold waters. These sharks are unique in their ability to elevate and maintain body temperatures above the ambient water temperature. They are endothermic. One striking feature of these warm-bodied sharks is that their flanks and viscera are warm, while the heart and gills are at environmental temperatures. This is because they differ substantially from all other sharks in the pattern of blood supply to the viscera and swimming muscles.
As in humans, sharks have a closed circulatory system in which arteries carry blood away from the heart and veins toward the heart. After blood leaves a shark's heart, it is pumped forward and upward to the gills. At the gills' secondary lamellae, carbon dioxide is dumped from the blood and oxygen is picked up, losing about 45% of its initial pressure as it passes through these delicate gas-exchange filaments (which may explain why many otherwise healthy sharks appear to 'go limp' when turned upside-down: shark systemic blood pressure is so low that, when inverted, the weak force of gravity changes blood distribution so that the brain and swimming muscles become starved for oxygen). From there, the freshly oxygenated blood is pumped fore to the head and aft to the rest of the body. The body's main blood supply in most sharks is the dorsal aorta, which extends beneath the backbone and from which radiate arterial branches that deliver oxygenated blood to the shark's fins, swimming muscles, and viscera. Deoxygenated, carbon-dioxide rich blood is collected from the internal organs and pumped forward back toward the heart via the abdominal and other veins.
The warm-bodied lamnoid sharks, however, have a special organ in their circulatory systems that allows them to retain much of the heat generated by swimming and other metabolic activity. In cold-bodied sharks, this heat is radiated from the body surface and lost to the environment. Warm-bodied sharks are able to greatly reduce this heat loss by redirecting blood from enlarged arteries along the flanks inward through a dense bundle of small arteries and veins called the rete mirable (pronounced 'REET meer-ah-blay', which means "wonderful net"). The arteries in each rete carry cold, oxygenated blood from the gills, while the veins carry metabolically-warmed, deoxygenated blood. These small arteries and veins pass very close to one another, carrying blood in opposite directions. Because of this intimate countercurrent blood flow, most of the heat is transferred from the veins to the arteries and cycled back to the muscles and visceral organs that produced it originally. The warm-bodied lamnoid sharks have three sets of retia: one in the swimming muscles, another in the anterior viscera, and a third surrounding the brain. Lamnoid sharks with this modified circulatory system are able to maintain body temperatures well above that of the water in which they swim. Recent studies by shark biologist Kenneth Goldman and his co-workers off South Farallon Islands, California, revealed that the White Shark is the warmest of the lamnoids, having a stomach temperature measuring as much as 25° Fahrenheit (14° Celsius) above the ambient water temperature.
The advantages of being warm-bodied are stupendous. An 18° Fahrenheit (10°C) rise in body temperature can result in a three-fold increase in the speed and strength of muscle contraction — providing more power from a given muscle mass. For the Great White and other lamnid sharks, this may afford an increase in sustained swimming speeds. Greater speeds may be selectively advantageous when chasing prey or fleeing from predators (although it is difficult to imagine anything — other than man — regularly preying on even moderately large lamnoids). The rete 'brain heater' may help the White Shark remain alert in the mind-numbing chill, helping to stave off the grogginess brought on by their cold-water environment. Elevated visceral temperatures — which are highest in the stomach and intestinal valve — may allow warm-bodied lamnoids to increase the rate of digestion and absorption of food, making available more caloric energy per day. In an intriguing 1987 paper, ichthyologist John McCosker reported that the stomach temperature of a free-swimming 11.5-foot (3.5-metre) White Shark off South Australia fell dramatically after consuming a transmitter hidden in bait (probably due to the influx of cold ocean water during swallowing) but rose quickly afterward, demonstrating that the shark was generating and retaining heat that warmed its stomach. McCosker found that the stomach of his unwitting research subject measured as much as 13.3° Fahrenheit (7.4° Celsius) above the ambient water temperature. Conservation of body heat may grant the White Shark a more complete conversion of thermal energy to work — or, to put it informally, more miles-per-fish.
The visceral retia also warm the uteri of endothermic sharks. By holding their young in warm uteri, lamnoid sharks may somehow enhance the development of their embryos. Perhaps this shortens gestation, increasing the number of pregnancies a warm-bodied shark may have over her lifetime. Unfortunately, we know so little about development in these sharks that their gestation periods cannot be compared with those of cold-bodied sharks. Being warm-bodied probably also allows the Great White and the other warm-bodied sharks to make excursions into colder or deeper waters, taking advantage of the rich feeding found there. A fascinating 1993 paper by physiological ecologist Barbara Block and her co-workers examined the phylogeny and retia mirablia of active, warm-bodied teleosts such as tunas and billfishes (which have a retial system that is similar — but not identical — to that found in lamnoid sharks). Block et alii's results strongly suggest that the primary selection pressure fostering the evolution of endothermy in these fishes may have been range extension into cold waters rather than increased aerobic activity. Thus, the White Shark may benefit most from being warm-bodied not by being able to swim faster or digest food more quickly and completely, but simply by being able to function efficiently in cold water where ectothermic sharks cannot compete with it.
But the advantages of endothermy are costly. Theoretically, a warm-bodied shark may need more than ten times as much food as a cold-bodied shark of the same size. One would therefore expect that — to maintain a warm body in cold water — a large, active shark must burn fuel like a blast furnace. The thin biomass of tropical seas cannot readily support such a high-energy carnivore. Since cold temperate inshore waters offer large fishes and large, energy-rich marine mammals, warm-bodied lamnoid sharks are most abundant in these areas. The distribution of warm-bodied sharks is thus dictated largely by availability of prey. For example, the Great White is undeniably one of the sea's paramount predators: it can — and does — feed on virtually anything that swims. An influential 1984 paper by Tim Tricas and John McCosker found that off California, White Sharks larger than about 10 feet (3 metres) in length seem to specialize in feeding upon pinnipeds such as seals and sea lions. Pinnipeds are large, swift, and agile, representing a substantial if tough-to-catch food source. Most pinniped rookeries (large breeding colonies) are in cold temperate or sub-polar regions, and the White Shark rarely strays far from these important food sources.
While energetically expensive, endothermy has enabled some lamnoid sharks to function as effective predators in cold waters, taking advantage of the rich feeding available there. In the North Atlantic, Shortfin Makos pursue high-speed ocean rovers, such as bluefish and swordfish. The Salmon Shark is an endurance predator, picking off Pacific salmon as they migrate along the coasts of Alaska and northern Japan. The Bigeye Thresher swims deep in cold water, scanning the surface for the silhouette of schooling baitfish with its huge, upward-mounted eyes. The combination of large size, efficient metabolism, high-speed swimming, and powerful jaws help make the lamnoid sharks versatile predators, allowing them to feed on a broad spectrum of prey types. By extending their range into cold waters, these sharks avoid competition with their cold-bodied cousins, which must remain in warmer seas. No doubt the heat-retaining retia of the Great White and a few related sharks has freed them from being captives of the isotherms — allowing them to range throughout the breadth and depths of the World Ocean.
