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How Salmon Adjust from Fresh Water to Salt Water, and Back Again

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In the salmon sequence of Living Waters: Intelligent Design in the Oceans of the Earth, one of the stories documentary producer Lad Allen wanted to tell was about osmoregulation. That is, the control of body fluids and ions during the transition from fresh water to salt water and back again. This is an important transition in the life of every Pacific salmon.

Allen’s crew researched this fascinating topic, but in the final cut they only had time to mention it briefly, stating, “In preparation for their time at sea, these small fresh water fish must adapt their biology to survive in salt water, then enter an ocean they’ve never seen.” How exactly does it work?

Three main things must occur for the young salmon, called a smolt, to prepare for life in the salty ocean. First, it must start drinking a lot of water. Second, the kidneys have to drop their urine production dramatically. Third, and very important, molecular pumps in the cells of the gills have to shift into reverse, pumping sodium out instead of in. All these physiological changes have to change back when then the mature fish re-enters the freshwater river on its way to spawn. The fish will spend a few days in the intertidal zone as these changes are made automatically.

From a design perspective, the third change is very interesting. The gills contain specialized pumping cells called chloride cells. The membranes of these cells contain molecular machines with the bulky name, Na+/K+ ATPase. We’ll call them NKA for short. As the name implies, the machine spends ATP to operate on sodium (Na) and potassium (K) ions. This machine is important in all animal cells. In fact, they are at work in your brain right now. The Nobel Prize was awarded to Jens Christian Skou in 1997 for his discovery of NKA back in the 1950s. Wikipedia has some simplified diagrams of the pump.

NKA is essential for numerous functions. It helps control cell volume. It contributes to cell signaling. And it regulates the cell’s “resting potential” (or resting voltage), its default electrical charge from which modulations indicate activity, such as the spikes in neurons (see this short Neurotech video overview, and the Wikipedia discussion of the complexities of this operation). Here’s an interesting factoid: most animal cells spend a fifth of their energy on these pumps. Nerve cells, because they depend on ionic charges to transmit signals, spend two-thirds of their energy budget running their NKA pumps.

For all these functions, NKA has to regulate the amount of sodium and potassium inside the cell membrane. Because fresh water is low in sodium, salmon need their gill cells to pump it in as they swim downstream. But once they enter the ocean, sodium is overly abundant, requiring them to pump it out. Salmon also have to pump out the chloride ions (Cl-) that result from dissolved ocean salt.

It would have been fun in Living Waters to have Illustra’s talented animator Joseph Condeelis produce another animated sequence showing how NKA works. Fortunately, there are some animations online that, while of lesser quality, demonstrate this important function for animals in general. Here is a very simplified 90-second clip on the basic action of NKA by John Munro on YouTube. All this shows is that three sodium ions are pumped out for every two potassium ions pumped in, both ions going against their concentration gradient. The machine resets automatically, spending one ATP for each cycle. As with most molecular machines, the details are, of course, much more complicated.

If you can forgive the lame production and boring narration, another animation from pittbiostudent’s YouTube channel is more informative, showing the shape of the protein machine and the detailed conformational changes it undergoes during transfer of sodium and potassium ions, You can browse the 9-minute video to your taste; the mechanism of action begins at 4:00.

Now that you have the basic operation in mind, remember that these machines work extremely rapidly in a coordinated fashion. In salmon, special chloride cells are networked with accessory cells in “a mosaic of interlocked cell processes bound together by an extended, shallow apical junction” (PubMed). Scientists have identified two distinct forms of the chloride cells in salmon, one for fresh water and another for salt water (Journal of Experimental Biology).

A short article by E. Toolson of the University of New Mexico explains how salmon regulate their fluids and ions despite radical changes in their environment. It’s a daunting problem:

Like nearly all vertebrates, the salmon is an excellent osmoregulator. However, like virtually all osmoregulators, the salmon is never in true equilibrium with its surroundings. As you can see from Row #1 in the accompanying table, in the ocean, the salmon is bathed in a fluid that is roughly three times as concentrated as its body fluids, meaning that it will tend to lose water to its surroundings all of the time. And, because the composition of its body fluids is so different from the ocean water, the salmon will be faced with all manner of gradients that are driving exchanges that will continuously tend to drive its body fluids’ concentration and composition beyond homeostatic limits. In particular, the very high concentration of NaCl in the ocean water relative to its concentration in the salmon’s body fluids (see Row #2 in the above table) will result in a constant diffusion of NaCl into the salmon’s body. Unless dealt with effectively, this NaCl influx could kill the salmon in a short time. In sum, a salmon in the ocean is faced with the simultaneous problems of dehydration (much like a terrestrial animal, such as yourself) and salt loading.

However, if fresh water, the problem is basically reversed. Here, the salmon is bathed in a medium that is nearly devoid of ions, especially NaCl, and much more dilute than its body fluids. Therefore, the problems a salmon must deal with in fresh water environments are salt loss and water loading. [Emphasis added; italics in the original.]

Toolson briefly discusses how the salmon drink more water and concentrate their urine when entering the ocean, but then spends his best praise describing the NKA pumps. These molecular machines work overtime to keep the fish “out of equilibrium” with its environment, so it can survive:

The final adaptation that we’ll discuss is a remarkable one that salmon use to deal with the NaCl fluxes driven by the gradients between the salmon and its surroundings. In their gill epithelial cells, salmon have a special enzyme that hydrolyzes ATP and uses the released energy to actively transport both Na+ and Cl against their concentration gradients. In the ocean, these Na+-Cl ATPase molecules ‘pump’ Na+ and Cl out of the salmon’s blood into the salt water flowing over the gills, thereby causing NaCl to be lost to the water and offsetting the continuous influx of NaCl. In fresh water, these same Na+-Cl ATPase molecules ‘pump’ Na+ and Cl out of the water flowing over the gills and into the salmon’s blood, thereby offsetting the continuous diffusion-driven loss of NaCl that the salmon is subject to in fresh water habitats with their vanishingly low NaCl concentrations.

Adding to all that complexity, the fish must have, in advance, the behavioral instincts that keep it from charging out into the sea before its body is ready. Through it all, the fish’s body fluids and ion concentrations are kept within tight specifications, allowing its muscles, nerves, senses and all its other systems to work properly.

We hope this brief survey of osmoregulation in the Pacific salmon enhances your appreciation of their multiple design features as shown in Living Waters. Add this to the film’s beautiful depictions of their life cycle, navigation, and remarkable sense of smell. Even then, a full accounting of the salmon’s design has only begun.

Image credit: Illustra Media.

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