Fish Out of Water

Fish that can breathe air? Walk on land? Yes, and they also provide clues to an evolutionary mystery

10-01-1994 // Caroline Harding

Early in the Devonian Era, nearly 400 million years ago, all the continents were grouped closely together and surrounded by sea. The climate ranged from periods of dry weather to periods of torrential rains, much as parts of the tropics do today. No flowering plants blossomed on land, for flowers had yet to evolve. No vertebrates--animals with backbones--walked the Earth, for those creatures that existed were entirely aquatic.

In this lost era, evolution was in the process of taking a major step. Most of the fish species of that distant time possessed lunglike organs that, in later fish species, would evolve into swim bladders to control buoyancy. Many of these lunged fishes moved on lobed fins, fleshy appendages that could support fish body weights as they crawled underwater.

For reasons about which scientists can only speculate, some of these fishes applied their lungs and lobed fins to new tasks: the lungs to breathing air, the fins to walking on land. As generations passed, the creatures became increasingly adapted to terrestrial life. They gave riseeventually to the amphibians, true land animals with fully developed legs, and led ultimately to reptiles and dinosaurs, birds and us.

The earliest stages of the trek up the shore apparently took place in habitats poorly suited to the preservation of fossils, so scientists can only guess as to how the transition actually happened. However, today several species of amphibious fishes thrive along sea coasts around the world, from California tidepools to muddy Southeast Asian mangrove forests. Some scientists believe these "land fish," capable of surviving in air for extended periods, provide clues to the mystery of how vertebrates first invaded the land. "These fishes are at an ecological, evolutionary transition point," says Jeffrey Graham, director of Scripps Institute of Oceanography's Physiological Research Institute. "They're moving from one environment to another and hold an intellectual promise of being a model of what the evolution from water to land might have been like."

Those ancient species that first set fin on terra firma must have done so for several reasons. The shore may have offered the creatures a chance to broaden their diets-by seeking food both in water and on land the fish could add insects and other land invertebrates to the aquatic creatures they already preyed upon. Ironically, the shore could also offer amphibious fishes a refuge from the sea creatures that preyed upon them. Finally, shoreline fish that could convert to breathing with lungs had a better chance of surviving exposure to air, such as when washed ashore or when trapped in isolated pools at low tide.

Experiments with today's air-breathing pisceans support this speculation about the odyssey from water to land. Back in the late 1960s, when Jeffrey Graham was a doctoral student with a research fellowship at the Smithsonian Tropical Research Institute in Panama, he discovered that if he sat on the steep, rocky shore of Culebra Island in Panama Bay, he could watch amphibious rock-skipper fish come out of the water to feed. In fact, he could feed them himself. When he threw pieces of barnacles onto the slippery rocks, the 6-inch-long rock-skippers would dash out of the sea, grab a piece of barnacle meat and race back to the water. Did the land-lubbing fishes of 400 million years ago quest similarly for scraps of food washed on shore, fragments perhaps of dead sea creatures shattered on jagged rocks?

Graham also tested the hypothesis that the shore served as an escape route from predators. He put some captive rockskippers in an aquarium with a model shoreline and then placed several snapper fish in the tank. The fish then enacted a scene that might have occurred early in the Devonian. "The snappers swam over and tried to eat the rockskippers," he explains, "but when the rock-skippers saw them coming, they turned around and 'walked' up on land."

Today's amphibious fishes also show how air-breathing can be a distinct benefit to fish trapped in shrinking bodies of water or in pools with dropping oxygen content, dangers that Devonian shoreline fish must have faced. Karen Martin, a doctoral student at the University of California, Los Angeles, discovered this when she initiated studies in 1990 on Southern California's most common tide-pool fish, the woolly sculpin. This fish belongs to a family that includes more than 100 North American salt- and freshwater species, many of them specialized for life in rocky intertidal zones.

Interested in finding out how the fish survive in tidepools at night, when plants have stopped photosynthesis and oxygen levels in tidepool water drop severely, Martin set up an aquarium with a shore-like ramp and lowered the water's oxygen concentration. At first, the creatures responded by pumping more water through their gills. But as the oxygen level continued to dip, they began moving up the ramp and obtaining oxygen from the air. Presumably, the fish would also move to land in the wild, where they might even be able to wend a path to a larger, more oxygenated pool. Jeffrey Graham's rockskippers also were quick to leave the water when he lowered the oxygen level in his laboratory tanks. "It's a very sudden and dramatic transition," Graham says.

The success that early fish species had on land would have depended in part on how long they could breathe air. The longer they could do so, the greater their chances of avoiding determined predators or of finding fresher waters. Doubtless, some species were better at air breathing than others. Today, for example, the rockskipper that Graham has studied usually makes only short forays onto land, "walking" by curling its tail up toward its head, extending flattened pectoral fins, lifting up on stout pelvic fins and flexing its tail back and forth to either side of its head. It spends about half its life out of water, remaining on land for as long as 20 minutes at a time.

Other fish, however, spend more time on land and, consequently, require better adaptation to life out of water. The sculpins that drew Martin's interest can breathe air for 24 hours, though they infrequently come completely out of water.

Malcolm Gordon, a physiology professor at the University of California, Los Angeles, discovered that mudskippers, small amphibious fish from East Africa and China, could survive in air for as long as two and a half days. They are also amazingly agile, scrambling over rocks, jumping from one mangrove root to the next and skipping about on moist shores. When resting, they often gather in small groups, sometimes latching on to upright mangrove roots with their pectoral fins or even sitting on the open shore. A University of Arizona graduate student, William Eger, found that four clingfish species in the Gulf of California could survive in air for remarkably long periods, in excess of three and a half days.

The differing amounts of time that various species spend onshore affect their ability to use terrestrial habitats and suggest that Devonian fishes, too, must have differed in their level of adaptation to land, with some species using land more successfully than others. Michael Horn, a biology professor at California State University, Fullerton, examined the onshore lives of five species of monkey-faced pricklebacks-slender, eel-like fishes that live in crevices and holes in shallow rocky areas from the Oregon coast to Baja California. He discovered that each species has a different tolerance to desiccation and that some can survive in air for as long as 36 hours. Those best able to withstand water loss inhabit the upper reaches of the beach, and those with the lowest endurance stay nearest the water. "Different species have different vertical distributions on the shore," he says. "It's not as if it's an occasional stranding and then tomorrow you find another species there. It's predictable. They are specialized for being there."

When today's amphibious fishes come on land, they generally use their gills to breathe air. This contrasts with the Devonian species, which could have used their lungs. Woolly sculpins, when on land, obtain 71 percent of their oxygen through their gills and oral membranes and 29 percent by breathing through their skin, called cutaneous respiration. Sculpins ventilate their gills at a slower, more irregular rate in air than in water. Because air contains about 20 times more oxygen per unit volume than water, the fish still absorb the same amount of oxygen. "It's actually more efficient for them to get the oxygen from air because it's more available and less energetically expensive to get it," says Martin.

The gills of amphibious fishes are larger than those of purely aquatic species. The increased size facilitates the gills' ability to take oxygen from the air. Gills are made up of rows of long, stringlike filaments composed of thousands of miniature, capillary-rich structures called lamellae, which absorb oxygen from surrounding media. The lamellae of most fishes have support rods, but those of amphibious species are thicker and prevent the structures from collapsing during land excursions.

Some amphibious fish species supplement the respiratory activities of their gills. Mudskippers carry a small volume of water in their mouths and gill chambers while on land. Malcolm Gordon believes that the water makes respiratory gas exchange possible and helps maintain body fluids. During brief visits back to their mudburrows, the fish dip their mouths into the water for a refill.

While mudskippers seem to be taking a piece of the aquatic world on land with them, other amphibious fish species seem to have made a complete switch to air breathing. Eger, while researching four clingfish species that live in the Gulf of California, learned that the fish breathe simply by taking in air through the mouth and expelling it through gills. The gas they expel is carbon dioxide, the same gas that humans and other land vertebrates exhale. Martin, who has studied 12 species of California intertidal fish, was amazed to find that they, too, could eliminate carbon dioxide on land. "In that regard, they are basically being terrestrial animals," she says.

This is not the only unexpected physiological adaptation found in amphibian fishes. Gordon was surprised to find that in mudskippers the heart and metabolic rates-and even the blood lactic-acid levels, which indicate when a fish is running out of oxygen and must resort to other energy sources-remain unchanged whether the fish is in water or air. This contrasts sharply with what scientists have observed in purely aquatic species. "Unlike an aquatic fish that jumps into the air and starts suffocating right away, these guys don't," he says. "They're able to breathe just as well in air as they are in water."

Amphibious fishes must be able to do more than merely breathe air. The terrestrial environment makes special biological demands even on fish that largely remain in small pools of water. "The water heats up, the rocks heat up, and the heat speeds up the drying," says Horn. "So not only a hotter but a more desiccating condition develops." Evaporation causes salt to be left behind and the salinity of tidepools to increase. Devonian land fishes more or less dealt with these problems by evolving into terrestrial species. For example, dry, scaly skin keeps reptiles from drying out on land, and special adaptations permit their eggs to develop out of water. Today's land fishes, of course, lack such high-tech terrestrial gear, but do well enough with the organs they have. Gills specialized for shifting between modes of sodium uptake or release allow intertidal fishes to adjust to changing salt concentrations in environments lethal to open-ocean fish species.

The amphibious fish's sensory world also shifts when the animal leaves water, requiring an evolutionary restructuring of some sense organs. For example, purely aquatic fish cannot see out of water, just as we cannot see underwater. Most fish are myopic in air because their curved corneas (the transparent layer over the eye) and their spherical lenses (which focus images on the light-receptive retina at the back of the eye) do not work out of water.

But semi-terrestrial fishes possess adaptations for vision in air. In rockskippers, Graham found, flat corneas compensate for the difference in the density of air. The corneas also are divided into anterior and posterior windows that enable the fish to see clearly. When the fish emerge, excess water droplets drain through grooves in each window.

Mudskippers, on the other hand, have protruding eyes that move independently of each other, muscles that raise or lower them and water-filled cups into which the fish dip their eyes while on land. They have flattened lenses and curved corneas that combine to focus sharp images in air.

Although the life histories and adaptations of today's amphibious fishes give us a sense of how vertebrates made the shift from sea to shore, it is unlikely that these creatures will give rise to future terrestrial species. "The main difference between amphibious fishes and the fishes which once gave rise to the amphibians and reptiles and us is that today there are animals living on dry land," says Carl Gans, a Michigan biologist. "So while these fishes may get into the amphibious niche, once they go onto land, they are competing with specialists." So then, should modern amphibious fishes be written off as an evolutionary dead end? Not exactly. Says Malcolm Gordon, "You can hypothesize that if for some reason life on land were to cease, then there is the possibility of reinvasion. In that light, you can look at existing amphibious fishes as being an evolutionary insurance policy."

Los Angeles writer Caroline Harding's last article for National Wildlife was about diving sea creatures.

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