Short answer: Cutaneous respiration (breathing through their skin) and storing lactic acid in their shell.
While reading about green anoles and “hibernation” yesterday, I came across this intriguing line from Vitt and Caldwell’s Herpetology and felt compelled to read more:
Survival [of painted turtles during hibernation] is possible because of high tolerance for lactic acid buildup, which can be stored in the shell, and because their metabolic rate is reduced to 10–20% of their aerobic resting rate.
Painted turtles (Chrysemys picta) are the most abundant turtles in North America. There are four subspecies of the painted turtle, with the Western painted turtle being both the most colorful and common. Adult females are larger than adult males (10-25 cm vs 7-15 cm, weight 500g vs 300g). Painted turtles are named for their coloration and have red, orange, and yellow stripes found on their heads, necks, and tails. These turtles can live a long time – more than 40 years in the wild!
Painted turtles live in slow-moving freshwater. They bask for warmth on logs or rocks in the warmer seasons. In the winters, they hide and hibernate in the muddy bottoms of their freshwater habitats. Like many other reptiles, the sex of the hatchlings is determined by the temperature of the nest during the middle third of the incubation period (22-26 degrees C for males, >28 degrees C for females). Of course, global warming hurts these turtles’ chances for reproduction by causing more and more hatchlings to be female.
The hibernation of painted turtles is particularly interesting – they can survive in freezing waters (as low as 3 degrees Celsius) without oxygen for months at a time. Cold and anoxic environments allow the turtle to use a fraction of the energy of a similarly-sized aerobic mammal (e.g. < 0.01% of the ATP usage of a comparably sized rat). There are 2 possible limiting factors for the survival of a turtle facing such prolonged anoxia: 1) depletion of glycogen reserves and 2) buildup of lactic acid (a byproduct of anaerobic metabolism). As noted in the figure above, painted turtles can use as little as 0.01 kcal/kg/min in anoxic, cold environments. For a 500g turtle, this amounts to only 7.2 kcal/day. Painted turtles have high glycogen content in their livers, skeletal muscles, and heart – these stores are sufficient at this level of energy expenditure for the average turtle to last for 5.5 months! Clearly then, the major hurdle facing the anoxic turtle is the buildup of lactic acidosis.
Painted turtles can build up plasma concentrations of lactic acid as high as 200mM (by contrast, a normal level in humans ranges between 2-4 mM). The painted turtles counteract this phenomenon in several ways:
- Direct body fluid buffering – painted turtles have high baseline plasma bicarbonate concentrations (40mM), with periotneal and pericardial fluid having concentrations of 80-120 mM.
- The turtle’s shell. The shell may release calcium carbonate, allowing for further buffering. In addition, lactate may be directly sequesterd by the shell. The lactate can then be flushed out later in normoxic conditions. Even during hibernation, turtles can switch between a normoxic and anoxic states (which may explain turtles swimming below the ice of frozen ponds). Apparently, this mechanism is not unique to the painted turtle, but generalizes to vertebrate bone, the carpace of crustaceans, and the shells of snails. As further proof, soft-shelled turtles fare much poorer in anoxic waters, lending more credence to the shell mechanism.
For those interested in more reading, I’d recommend looking into the work of Professor Donald Jackson. He passed away in 2020, but he seems to have written much of the seminal work on painted turtle physiology during his time at Brown.
As a final note, adult painted turtles cannot survive truly freezing temperatures (-1 to -2 degrees C). However, hatchling painted turtles can via supercooling – which I may discuss this further in the future… Also, stay tuned for a discussion tomorrow comparing turtle and human CPR!
- Vitt, L. J., & Caldwell, J. P. (2014). Herpetology: An introductory biology of amphibians and reptiles. Pages 203-227.
- Taking the temperature of the painted turtle. Lab Anim (NY). 2013 Sep;42(9):315. doi: 10.1038/laban.376. PMID: 23965557.
- Jackson, D.C. Hibernating without oxygen: physiological adaptations of the painted turtle. J. Physiol. 543, 731–737 (2002).
- Jackson DC. How a Turtle’s Shell Helps It Survive Prolonged Anoxic Acidosis. News Physiol Sci. 2000 Aug;15:181-185. doi: 10.1152/physiologyonline.2000.15.4.181. PMID: 11390905.