How do waterdwelling turtles survive the winter?

An anaerobic adventure

Living in freshwater seems fun until winter. Then your pleasant, watery home becomes ice, and you have to change up your entire living strategy.

If you’re a fish, frog, or other animal that can breathe underwater, you can just go to the deepest parts of your lake and go into torpor, barely moving and taking in very little food or oxygen. This presents its own challenges, like not freezing and still getting enough water over your gills to get oxygen (for fish, at least), but it’s doable. 

If you’re a painted turtle, however, you can’t do that¹. Even though you’re a water-dweller, you can’t breathe underwater², so torpor isn’t an option. You have to go up to the surface to breathe. That’s fine in every other season, but, in winter, the entire water surface might be covered in ice. Even if it’s not, swimming in freezing water to find gaps in the ice to breathe is an energetically costly process during a time when food is scarce.

So what do you do? Well, you might think you should go on land. But painted turtles take a different tact. They still go underwater (or under the mud). However, they don’t go into torpor. They go deeper, into an even lower metabolic state of hibernation, and stop breathing completely for the entire winter.

This is from a Youtube video entitled “Turtles Under Ice! How? Why?” I like how excited this guy is.

If that sounds like a crazy physiological adaptation to you, it is! Not breathing for months at a time is really hard. Turtles, like all animals, like oxygen. During the summer, they need it. During the winter, they don’t. Let’s talk a bit about why.

If you remember from AP Biology, oxygen’s main use in the body is for aerobic respiration, which occurs in the mitochondria. Basically, our mitochondria use oxygen’s hunger for electrons to drive the creation of ATP, the short-term energy storage of the body. The more short-term energy we use, the more oxygen we need. This is why you breathe hard when you run.

Most animals have a secondary³, anaerobic process when aerobic respiration is not enough to provide all of the body’s energy needs, called lactic acid fermentation⁴. This is not a great secondary option. Not only is it not particularly efficient, but it leaves behind a waste product, lactic acid.

Lactic acid is bad for you. It’s an acid, which means it attacks tissues, and it builds up in your bloodstream, lowering the pH and disrupting your cells. Plus, it just feels terrible. It causes burning and anxiety, and may, in fact, be an underrecognized cause of panic attacks⁵.

For humans, the problems caused by lactic acid buildup are so serious that we can’t go long without breathing, even if we’re not expending a lot of energy. When we do have too much lactic acid, we tend to go into lactic acidosis⁶, which if it lasts long enough, can lead to death.

Painted turtles aren’t immune to lactic acid. However, they do have something we don’t: shells. During the winter, their shells (and maybe bones) release calcium and magnesium into their bloodstream. The calcium and magnesium react with the lactic acid, forming calcium lactate and magnesium lactate salts. They then store these salts in their shells (and maybe bones). One study found that 40% of one painted turtle’s shell was calcium lactate.

A turtle shell from Wikipedia. You’ll notice that the shell is built from the bottom up, generating new scales from a keratin lattice (and possible interstitial calcium and magnesium lactate). This pushes up the old scales, which are dried, hardened, and form the protective outer armor until they are eventually sloughed off.

So, turtles survive the winter by not breathing, and they survive not breathing by not moving and buffering and sequestering lactic acid in their shells and maybe bones. Neat, right?

1. I’m going to be talking about painted turtles because they’re the best studied, but these same adaptations probably hold for a number of air-breathing, aquatic turtles.

2. This isn’t entirely true. Painted turtles can breathe a bit underwater through their skin, but it’s an inefficient process. That’s why they still surface for air.

3. I’m probably going to write an article about lactic acid fermentation next, as I read a recent review paper that convincingly argues the story is much more complicated than the AP Bio version I relate here. I don’t feel like getting into the weeds in this essay, though.

4. Animals that don’t perform lactic acid fermentation include many invertebrates, some fish in low-oxygen zones, and parasitic worms. You’ll notice that all of these tend to live in low-oxygen environments, at least relatively low-oxygen in the case of invertebrates (i.e. they are bad at getting oxygen from the air to their cells, so normal air is low-oxygen for them). Instead, they tend to rely on alcohol dehydrogenase, so they excrete ethanol, much like yeast. This is apparently easier physiologically to deal with than lactic acid, which is surprising to me.

5. Lactic acid does not, however, cause delayed onset muscle soreness, despite what your gym teacher might have told you. DOMS is probably caused by direct strains on the muscle tissue.

6. Generally speaking, people don’t go into lactic acidosis because of a lack of supply of oxygen, though. If you lack oxygen, you’d probably die before then from brain death, because our brain requires too much energy to go without oxygen for very long. If you somehow avoided that, you’d also have an issue of inadequate oxygen-carbon dioxide exchange, leading to an excess of carbon dioxide (hypercapnia). 

Not only does hypercapnia lead to similar issues as lactic acidosis through an excess of carbonic acid, but our body is also apparently pretty bad at distinguishing between carbon dioxide and oxygen for most purposes. Both the brain and heart tend to have problems pretty quickly when dealing with high CO2 environments, even if there’s otherwise adequate oxygen. Turtles don’t have to deal with this in the winter because, even though they’re in a high CO2 environment, they’re not breathing it in.

People do go into lactic acidosis because of problems with oxygen delivery to the right cells or problems with aerobic respiration. In terms of problems of oxygen delivery, this can be as simple as a lack of blood supply (i.e. from bleeding) or shock causing vasoconstriction. In terms of problems with aerobic respiration, there are a bunch of interesting things that can go wrong with aerobic respiration.

So, for example, there are a number of different genetic conditions that affect the mitochondria in different ways and can mess them up badly enough to cause lactic acidosis. Some of these directly mess up the mitochondria, like Leigh syndrome, which causes the cell to develop messed up ATP synthase. 

Others of these mess up the mitochondria indirectly, like biotinidase deficiency. Biotinidase helps the body produce biotin from the food we eat. If the body can’t produce biotinidase, it has a deficit of biotin. Because biotin is a necessary cofactor for pyruvate carboxylase, pyruvate builds up in the mitochondria and is never converted to acetyl CoA. The only other way for it to leave is to be converted to lactate through anaerobic respiration, leading to lactic acidosis.

There’s also a number of different medications that can cause lactic acidosis. A fair number of these are antibiotics or antivirals, because some of those kill bacteria or viruses by interfering with the same sorts of processes mitochondria use. Cyanide, the poison that spies use to kill themselves in movies and sometimes in real life, also can cause lactic acidosis by directly inhibiting the electron transport chain, although, again, people tend to die due to lack of ATP in the brain and heart before lactic acidosis kills them.