How do you survive the cold of winter? Do you bundle up in your warmest jacket and mittens? Maybe you stay cozy in your toasty house. I bet you don’t rely on making antifreeze in your blood or exchanging oxygen using your…umm…butt!
Assuming you are a human reading this, you are an endotherm. That means that you control your own body temperature using your metabolism. This is opposed to being an ectotherm, which is when the temperature of the environment dictates body temperature. This is the case with reptiles and amphibians: cold seasonality equals cold body temperature. But what happens when the environmental temperature drops below zero?
To Freeze or Not to Freeze
Generally, letting your body temperature drop below 0℃ is lethal. This is because when tissue freezes, ice crystals form by taking water from the cells and causing them to dehydrate, resulting in cell death (Karow and Webb, 1965). This is not the case in some frog species, such as Wood Frogs, who can not only tolerate freezing, but can actually do it for 7 months of the year (Larson et al., 2014)! They do this by forming a glucose-based antifreeze, and dispersing it throughout their body. This allows the cells themselves to remain liquid, but the extracellular matrix to freeze (Duman, 2015), essentially creating a living frogsicle.
Wood Frogs can remain frozen solid for up to 7 months (Photo: Janet M. Storey)
Frogs aren’t the only herptiles that can stand the cold. Hatchling Painted Turtles also have adaptations to survive below zero. Rather than freezing solid, their body fluids stay liquid even when faced with freezing environmental temperatures. This is called ‘supercooling.’ This extraordinary phenomenon is possible because hatchling Painted Turtles lack ice nucleating agents (INAs), which are responsible for triggering the formation of ice crystals (Costanzo et al., 1998). No INAs, no ice formation. Painted Turtles often lay their eggs above the frost line at the end of the summer, and the hatchlings overwinter in their natal nest until spring. The body fluids of these hatchlings are capable of remaining liquid in environmental temperatures as low as -20℃ (Lee and Costanzo, 1998).
Hatchling Painted Turtles have a unique freeze avoidance mechanism called ‘supercooling’ (Frozen Planet II, BBC).
No Oxygen, No Problem
But what if freezing or supercooling isn’t an option? Well, you need to avoid the extreme cold. This is the case for the adult turtles of Ontario. They overwinter under the ice of ponds, where the temperature of the water remains stable and above the freezing point. However, there isn’t very much oxygen under the ice, so they need to lower their metabolic rate in order to reduce their oxygen requirements (Storey, 2007). When the water conditions under the ice become anoxic (deprived of oxygen), the turtles of Ontario differ in how they cope with this limiting factor based on whether they are anoxia tolerant or intolerant. The anoxia intolerant turtles (Wood, Map, Musk, and Spiny Softshell Turtles) navigate this obstacle by aggregating in high oxygen sites, and relying on breaks in the ice to come up for air (Robichaud et al., 2023).
It is the anoxia tolerant species (Blanding’s, Spotted, Snapping, and Painted Turtles) who really shine when it comes to mind-boggling adaptations. Specifically, it is the Painted Turtle who stands out in the crowd. Painted Turtles are known to use their cloaca (an organ used for waste excretion and reproduction) to uptake oxygen from the environment; a process called cloacal respiration. That's right, they use their butt! This is because the inside of the cloaca is full of blood vessels that make the perfect surface for gas exchange (you can read more about these butt-breathing antics here).
Ontario’s turtle species spend the winter under the ice of frozen water bodies (Wisconsin DNR).
The overwintering wizardry of Painted Turtles does not end there, however. In order for them to survive in oxygen depleted water, they need to switch to a type of metabolism that does not require it, called anaerobic respiration. This comes with a catch: anaerobic respiration creates a toxic byproduct called lactic acid (Jackson, 2000). This is the same byproduct that causes muscle cramps when we exert ourselves during exercise. In order to neutralize this build up of acid, they use carbonate from their shells (Jackson et al., 2007). This is comparable to how we take a Tums when we have too much acid in our stomachs, also known as heartburn.
Left in the Cold
Without these precious overwintering sites to meet the needs of our shelled friends living in the harsh northern winters, they would not survive (Freeman, 2022). Habitat destruction, specifically in the form of wetland filling and loss, results in turtles no longer having access to the overwintering site that they have relied on for years, causing them to succumb to the cold. Turtles create a spatial map of their home range at a very early age, becoming highly devoted to that area and unable to find their way through new environments (Roth and Krochmal, 2015). This is why turtles who are relocated to a new habitat are often unable to find a suitable overwintering site and are left defenseless in the face of predators and seasonal extremes.
Being committed to the protection of overwintering habitats is a big step toward keeping these butt-breathers and frogsicles safe at their northern range limit. To help, sign up to become a Citizen Scientist with Turtle Guardians!
Written by: Michaela S. Bouffard, Biologist, Road Ecologist, The Land Between and Turtle Guardians
Literature Cited
Costanzo, J. P., Litzgus, J. D., Iverson, J. B., & Lee JR, R. E. (1998). Soil hydric characteristics and environmental ice nuclei influence supercooling capacity of hatchling painted turtles Chrysemys picta. Journal of Experimental Biology, 201(22), 3105-3112.
Duman, J. G. (2015). Animal ice-binding (antifreeze) proteins and glycolipids: an overview with emphasis on physiological function. The Journal of experimental biology, 218(12), 1846-1855.
Freeman, H. C. (2022). Identifying Suitable Turtle Overwintering Habitat Through the Integration of Thermal, Chemical and Physical Wetland Properties.
Jackson, D. C. (2000). Living without oxygen: lessons from the freshwater turtle. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 125(3), 299-315.
Jackson, D. C., Taylor, S. E., Asare, V. S., Villarnovo, D., Gall, J. M., & Reese, S. A. (2007). Comparative shell buffering properties correlate with anoxia tolerance in freshwater turtles. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 292(2), R1008-R1015.
Karow Jr, A. M., & Webb, W. R. (1965). Tissue freezing: A theory for injury and survival. Cryobiology, 2(3), 99-108.
Larson, D. J., Middle, L., Vu, H., Zhang, W., Serianni, A. S., Duman, J., & Barnes, B. M. (2014). Wood frog adaptations to overwintering in Alaska: new limits to freezing tolerance. Journal of Experimental Biology, 217(12), 2193-2200.
Lee Jr, R. E., & Costanzo, J. P. (1998). Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology, 60(1), 55-72.
Robichaud, J. A., Bulté, G., MacMillan, H. A., & Cooke, S. J. (2022). Five months under ice: biologging reveals behaviour patterns of overwintering freshwater turtles. Canadian Journal of Zoology, 101(3), 152-162.
Storey, K. B. (2007). Anoxia tolerance in turtles: metabolic regulation and gene expression. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147(2), 263-276.