In 1928, a biologist named Ditlef Rustad caught an unusual fish off the coast of Bouvet Island in the Antarctic. The "white crocodile fish," as Rustad named it, had large eyes, a long toothed snout and diaphanous fins stretched across fans of slender quills. It was scaleless and eerily pale, as white as snow in some parts, nearly translucent in others. When Rustad cut the fish open, he discovered that its blood, too, was colorless—not a drop of red anywhere. The crocodile fish's gills looked odd as well: they were soft and white, like vanilla yogurt; in contrast, a cod's gills are as dark as wine, soaked in oxygenated blood.
Later, Johan Ruud and other researchers confirmed that the Antarctic icefishes, as they are now known, are the only vertebrates that lack both red blood cells and hemoglobin—the iron-rich protein such cells use to bind and ferry oxygen through the circulatory system from heart to lungs to tissues and back again. At first blush, biologists regarded icefishes' pallor blood as a remarkable adaptation to the Antarctic's freezing, oxygen-rich waters. Perhaps icefishes absorbed so much dissolved oxygen from the ocean through their gills and ultra thin skin that they could abandon those big, spongy red blood cells. After all, the biologists reasoned, thinner blood requires less effort to circulate around the body and saving energy is always an advantage, especially when you are trying to survive in an extreme environment.
More recently, however, some biologists have proposed that the loss of hemoglobin was not a beneficial adaptation, but rather a genetic accident with unfortunate consequences. Since icefish blood can only transport 10 percent as much oxygen as typical fish blood, icefishes were forced to dramatically alter their bodies in order to survive. In this scenario, despite an evolutionary blunder that would be lethal to most fish, the icefishes' grit—as well as a little ecological serendipity—rescued them from their own bad blood. Scientists continue to revise icefishes' evolutionary history as new evidence surfaces, but their story is surely one of the most unique and bizarre in the animal kingdom.
Icefishes live in the Southern Ocean, which encircles Antarctica. Rotating currents essentially isolate these waters from the world's warmer seas, keeping temperatures low: temperatures near the Antarctic Peninsula, the northernmost part of the mainland, range from about 1.5 degrees Celsius in the summer to –1.8 degrees Celsius in the winter. Many fish in the Southern Ocean, including icefishes, produce antifreeze proteins to prevent ice crystals from forming in their blood when ocean temperatures drop below the freezing point of fresh water. Sixteen species of Antarctic icefishes comprise the family Channichthyidae, which falls under the larger suborder Notothenioidei. Among the hundreds of red-blooded Notothenioid species, only the icefishes lack hemoglobin. Together, the Notothenioids and icefishes dominate the waters they call home, accounting for approximately 35 percent of fish species and 90 percent of fish biomass in the Southern Ocean.
By comparing icefish DNA to the DNA of red-blooded fish, William Detrich of Northeastern University and his colleagues identified the specific genetic mutations responsible for the loss of hemoglobin. Basically, one of the genes essential for the assembly of the hemoglobin protein is completely garbled in icefishes. Although no other vertebrate completely lacks red blood cells, biologists have observed a diminishing of red blood cells in response to a changing environment. When it gets cold, it's advantageous for fish to make their blood a little thinner and easier to circulate. Fish that live in cold waters usually have a smaller percentage of red blood cells in their blood than fish that live in warmer waters. And fish in temperate regions decrease the percentage of red blood cells in their blood each winter to save energy. Relying on these facts, some biologists assumed that Antarctic icefish evolved incredibly thin blood as an adaptation to the Southern Ocean.
Kristin O'Brien of the University of Alaska Fairbanks and her colleague Bruce Sidell (who is now sadly deceased) decided to test this assumption. In a paper titled "When bad things happen to good fish," O'Brien and Sidell first point out that, compared to their cousins the Notothenioids and other similarly sized fish, icefishes have larger hearts and blood vessels. Although icefishes pump unusually thin blood through their bodies, their circulatory systems handle huge volumes. O'Brien and Sidell calculated that icefishes expend approximately twice as much energy as red-blooded Notothenioids moving all that extra blood. Whereas fish in temperate zones devote no more than five percent of their resting metabolic rate to their hearts, icefishes invest a whopping 22 percent of their body's available energy in their giant tickers.* O'Brien and Sidell also show that icefish have more blood vessels nourishing certain organs than red-blooded fish. If you peel back the outer layers of a typical fish's eye and fill the blood vessels with yellow silicone rubber, you will see a web of neatly segregated vessels tracing the contour of the eye like the ribs of a pumpkin. Do the same to an icefish's eye and you will find a dense, tangled mess like a plate of spaghetti.
Like other biologists in recent years, O'Brien and Sidell view the icefishes' large hearts and capillaries, high blood volume and dense nets of blood vessels as compensations for the loss of hemoglobin. But these adaptations alone might not have been enough to save icefishes from extinction—they likely benefited from fortuitous circumstances as well. Around 25 million years ago, the Southern Ocean flowing around Antarctica—which had broken away from other continents—began to cool. Not only did the colder water offer more oxygen, it also killed many species that did not evolve antifreeze proteins or otherwise adapt to the cold, creating a frigid sanctuary that the icefishes and their relatives have dominated ever since.
Today, however, icefishes face a new threat: manmade climate change. The Southern Ocean is getting warmer and possibly more acidic and less nutritious. O'Brien says researchers have shown that adult icefishes are more sensitive to changes in temperature than red-blooded fish—they cannot stand the heat. If Ruud was right—that "only in the cold water of the polar regions could a fish survive that has lost its pigment"—then the ongoing changes to the Southern Ocean might be the icefishes' undoing. Consider this version of their story: icefishes evolved to survive sub-freezing temperatures in one of the most extreme environments on Earth, only to lose their red blood cells to a genetic accident; despite the mishap, they kept swimming, expanding their hearts and growing more blood vessels to get enough oxygen around their bodies; now, people are turning the Southern Ocean into a habitat for which icefishes are completely unsuited, forcing them to adapt once again or perish. Personally, I'm clinging to the hope that even if icefishes do not have any hemoglobin in their blood, they have plenty of resilience coursing through their veins.
*Source for cardiac energy investment: Hemmingsen, E. A. and Douglas, E. L. (1977). Respiratory and circulatory adaptations to the absence of hemoglobin in chaenichthyid fishes. In Adaptations within Antarctic Ecosystems (ed. G. A. Llano), pp. 479-487. Washington: Smithsonian Institution.