This post was adapted from an older magazine article the Kiley wrote in late 2017.

With each trip in and out of the snow encrusted Canadian waters, another layer of ice accumulated on my waders, forming a frigid exoskeleton around my legs. I knew from experience not to tie the laces of my boots tightly, and was thus spared the embarrassment of later needing to wait for the ice to melt by a fire in the restaurant lobby before being able to remove my wading gear and join my hosts for dinner. The loose laces technique was one I learned after two field seasons setting and checking traps through river ice in Vermont; tight laces often necessitated an hour of blasting the heat in our work truck to melt ice before I could finally kick off my footwear and peel out of my sweat-soaked neoprene waders. There were days during that project when temperatures dropped to -30C (-20F) and the wire mesh of our traps would freeze instantly to our skin every time we hauled one up from a hole in the ice; holes we insulated with Styrofoam and snow to lessen the odds they would refreeze overnight.

If someone asked what we were doing out there, looking for salamanders wouldn’t be anyone’s first guess. Setting traps through ice wasn’t exactly how I expected to spend my first two years as a herpetologist, but that was before I learned Mudpuppies (Necturus maculosus), large fully aquatic salamanders that retain external gills into adulthood, are actually most active in the winter months, even when water temperatures are near freezing. In the middle of winter, those days on which metal instantly froze to our wet hands turned out to be the days we had some of the highest capture rates. Hauling the salamanders up to the surface, however, risked exposing them to fatally cold air, so we took great care to make sure the salamanders never left the water and transported them in buckets to our truck where we could measure and tag the pups in relative warmth before returning them to the river.

Beneath the ice, Mudpuppies remain active all winter, foraging and searching for mates at near freezing temperatures. Most studies that involve sampling Mudpuppy populations take place in the winter as that is the easiest time of year to find them.

Winter in the northeast is by and large an off-season for herpetologists with more sanity than me. It is a good time to write grants, analyze data, and drink a nice stout by a fire, but there is truly a lot going on under the ice and snow for those willing to look. Husband and wife duo, Fred Schueler and Aleta Karstad, are two such people, and have hosted a public event called “Mudpuppy Night” every Friday all winter for over 20 years, which is what brought me north of the border that chilly evening. During these Mudpuppy nights, Fred, Aleta, and their guests use spotlights to search for Mudpuppies foraging in the shallows beneath a dam in southern Ontario. Mudpuppies, which are normally very elusive and difficult to find, congregate in the rapids beneath the dam, sometimes numbering in the hundreds. Exactly why Mudpuppies gather at this dam all winter is not certain, perhaps to forage on fish disoriented by the rapids, or maybe it is just the tendency of Mudpuppies to move upstream in the winter and the dam blocks their progression. Either way, the fact remains that Mudpuppies are most active and easiest to find during the winter throughout their range. On this occasion, my travel companion had failed to heed my advice regarding loose laces, and spent the first half hour of dinner thawing out in the lobby so as not to ruin the restaurant floor with his cleats. Rookie move. 

Mudpuppy Night in Southern Ontario attracts people from all over to come out and observe Mudpuppies on winter nights as they forage along the river's edge..

Winter is an extremely harsh time for reptiles and amphibians in colder climates. As cold-blooded animals, exposure to even mildly freezing conditions can be fatal. Many northern species find places to overwinter that protect them from freezing temperatures by burrowing underground. Others seek refuge from the freeze underwater, but need to survive with minimal access to oxygen or even complete oxygen deprivation for prolonged periods; conditions that would kill most mammals in a matter of minutes. Because Mudpuppies mostly live in fast-flowing water that holds oxygen throughout the year they are spared the harshest conditions winter has to offer, but other reptiles and amphibians do manage to survive freezing conditions and prolonged oxygen deprivation. The ways in which they do this are quite fascinating and I would love to share with you what I know about these remarkable survival strategies, starting with how some species survive freezing.

Adult Painted Turtles (Chrysemys picta) cannot survive freezing temperatures, but their young, which hatch in the fall and stay in the nest all winter, are regularly exposed to temperatures that would kill adults. As ectotherms that cannot generate their own body heat, you would think hatchling painted turtles that experience below freezing temperatures would freeze solid and die, but that is not the case. If you were to subject most reptiles to freezing temperatures, water inside the body would expand and freeze, cells would rupture, organs would be crushed, and sharp ice crystals would pierce and shred cell membranes. All of that would add up to a very dead animal, but hatchling Painted Turtles have two methods of coping with freezing temperatures. The first line of defense is the hatchling’s ability to supercool, a process by which liquids in the turtle’s body drop to well below their normal freezing points without actually freezing. They do this by storing extremely high concentrations of glucose and other cryoprotectants (compounds that protect tissue from freezing conditions) between the cells within their bodies. High glucose concentrations drastically lower the temperature at which liquids inside the turtles freeze and the hatchlings can drop to below -10C (14F) without freezing. Interestingly, the moisture and soils surrounding the nests can impact the temperature to which turtles can supercool. In wet sandy soils, turtles can only supercool to about -2C (28F) before freezing takes place, but in clay soils they can chill to at least -13C (9F). This difference has to do with how ice crystals form in the different substrates. At such cold temperatures, if the turtles come into contact with ice for any reason, that contact essentially seeds the crystallization process in the turtles and causes a chain reaction whereby the turtles freeze solid almost instantaneously. In laboratory experiments with no outside ice to seed the turtle crystallization, hatchling Painted Turtles can supercool to -20C (-4F) before flash freezing occurs.

Hatchling Painted Turtles hatch in the fall, but overwinter in the nest and can survive most of their tissue freezing.

While freezing solid at -10C (14F) almost always causes turtle death, the hatchlings are tolerant of freezing at milder temperatures. The same glucose that helps the turtles supercool also protects their tissues from damage caused by the freezing process. High concentrations of glucose between the cells draws water into the extracellular spaces so when freezing does occur, it occurs outside of the cells and the ice does not rupture the cells as it expands. Consequently, the hatchlings can survive freezing to about -4C (25F). In this state, all but the liver and other vital organs freeze solid and can remain so for several days without causing harm to the turtles. Only a small handful of turtle species can freeze as hatchlings, and of those, only the Box Turtle (Terrapene carolina) can also freeze as an adult (Box Turtles being the only species with freeze-tolerant hatchlings that overwinters on land as an adult). The only other reptiles native to North America with some freezing ability are gartersnakes (Thamnophis sp.).

While they can only survive body freezing for hours at a time, that is enough to allow Gartersnakes to push the limits and emerge from their hibernacula very early in the year, even when there is still snow on the ground.

Gartersnakes are capable of supercooling to about -5C (23F) and can only survive in a frozen state only for about 10 hours or so. While this pales in comparison to abilities of the Painted Turtle, gartersnakes do not need to endure conditions nearly as extreme as those suffered by the turtles, in part because all gartersnakes, including neonates (newborns), overwinter far enough below ground to avoid freezing temperatures. Likely their tolerance of short periods below freezing is an evolved safeguard to protect against overnight frosts that might occur in the spring and fall when the snakes are above ground. This gives gartersnakes major advantages over other snakes and may explain why they range so much farther north than other species (by roughly 700 miles) and can be seen mating while there is still snow on the ground.

There are also a handful of amphibians with remarkable tolerance to freezing temperatures, and they make the freeze-tolerant reptiles look like amateurs. Across the world, only nine known species of frog can survive freezing and seven of them reside in North America: Gray Treefrogs (Hyla versicolor), Cope’s Gray Treefrogs (H. chrysoscelis), Pacific Treefrogs (H. regilla), Spring Peepers (Pseudacris crucifer), Boreal Chorus Frogs (P. maculata), and Wood Frogs (Lithobates sylvaticus). The mechanism by which they survive freezing is very similar to that of hatchling turtles; they produce sugars that draw water out of their cells so that freezing occurs outside of cells rather than within. The frogs aren’t prepared to freeze year-round, however, and only begin producing those excess sugars after being exposed to ice crystals in the fall (popping a Wood Frog into the freezer mid-summer does not typically have the intended results, as the parents of many curious children have discovered over the years). In addition to glucose, the treefrogs also use glycogen as a cryoprotectant and Wood Frogs retain urea (the frog equivalent to urine) to aid in the process.

Some frogs in the north, including this Wood Frog, can survive freezing almost completely solid.

During a freeze, frogs will appear from the outside to be entirely frozen. Their skin and eyes will be rock hard and most of the fluid in their bodies will be solid, but as with the hatchling turtles, their liver and heart remain in a super-cooled state. As temperatures drop and the frogs begin to freeze, their skin freezes first and the ice gradually moves inward towards the frog’s core until reaching those organs with such high loads of cryoprotectants that the freezing process halts (of course the liver and other vital organs eventually can freeze, killing the frog in the process). The heart will cease to beat for the duration of the freeze, until the thawing process when something truly remarkable happens.

If the frog’s tissues and organs thawed in the same order that they froze (outside to inside), the frog would die. The skin, limbs, and eyes would thaw out while vascular tissue connecting them to the heart was still frozen and tissue on the frog’s exterior would become necrotic before the core of the frog even thawed. Instead, the frogs thaw from the core outward, starting with organs that have the highest concentrations of sugary antifreeze. The heart starts beating and as each subsequent layer of tissue thaws blood flow is immediately restored until finally the skin and eyes soften. The entire process just takes a couple hours and the frogs can resume normal body function immediately afterward. 

Gray Treefrogs can also survive freezing almost completely solid.

Freeze-tolerant frogs can typically survive lower temperatures and remain mostly frozen for longer periods of time than any reptile, with most of them capable of freezing to roughly -5C (23F) or so for durations of up to a couple weeks. Recently, however, researchers found that Wood Frogs in Alaska near the northern extent of their range can survive freezing to temperatures as low as -18C (0F) and remain frozen for upwards of 200 consecutive days, which is an order of magnitude longer than anyone had previously documented. Those Alaskan frogs also had muscle glucose concentrations approximately ten times higher compared to Wood Frogs studied in farther south, suggesting the degree to which Wood Frogs can survive cold temperatures might vary according to latitude, as is the case with some insects. Throughout their range, however, air temperatures regularly fall far below that which the frogs can survive and frogs depend on insulation from snow cover to protect them from the harshest conditions. At the end of winter, that same snow serves another valuable purpose to the frogs.

Wood Frogs almost always breed and lay their eggs in vernal pools, which rely largely on snow melt as a water source in the spring. As temporary bodies of water that dry out by mid to late summer, vernal pools are free of fish that would prey upon breeding amphibians, their eggs, and their larva. For that same reason, amphibians need to lay their eggs as early in the season as possible if the young are to survive long enough to mature before pools dry. By overwintering close to the surface and enduring freezing conditions, Wood Frogs and other freezable species “wake up” at the earliest signs of spring and can migrate to the vernal pools as soon as the snow melts and long before other species, such as toads, emerge from their deeper winter refugia.

Because vernal pools where many amphibians breed will dry out most summers, being able to survive freezing allows several species to overwinter under leaflitter and migrate to the pools while much of the ground is still covered in snow.

So far I’ve only mentioned North American species, but avoiding Siberian Salamanders (Salamandrella keyserlingii) in a discussion about freeze-tolerant amphibians would be unforgivable. Siberian Salamanders use glycogen as a cryoprotectant, as do the treefrogs discussed earlier. Concentrations of glycogen in the Siberian Salamander are much greater than in the treefrogs, however, and they can survive most of the liquid in their bodies freezing down to about -55C (-67F), far lower than any other vertebrate, and three time as far below freezing as the Alaskan Wood Frogs. They can also remain frozen at somewhat milder temperatures (-35C; -31F) for up to 45 days, which apart from Alaskan Wood Frogs, is much longer than any other amphibians can survive in a frozen state, but presumably they can survive frozen even longer at warmer temperatures. Interestingly, while the Siberian Salamanders are frozen, a common source of mortality is sublimation (water in their tissue turning from a solid directly to a gas, which causes the salamanders to desiccate) rather than tissue damage caused by the extreme temperatures.

Freezing is by no means the only difficult condition winter has to offer. Many species of reptile and amphibian overwinter underwater in lakes, rivers, and ponds. Waterbodies, especially those with low flow, often completely ice over in the north, which is problematic. Ice creates a barrier that essentially traps the animals underwater and prevents them from reaching the surface to gulp air, but that in itself is not a problem for the species that overwinter underwater. Painted Turtles, for example, which spend winters underwater as adults, drop to the same temperature as the water, barely above 0C (32F), and at such temperatures their metabolisms drop by about 95%. This means their oxygen demands are so low they can get all the oxygen they need by respiring through their skin, especially the skin inside and around their mouth and cloaca (the non-jargon term for this is “butt breathing”). Painted Turtles will spend most of the winter buried under leaves and sediments, but will occasionally move around and can even be seen swimming under the ice. That is, until, oxygen levels in the water crash, a condition called anoxia, which is a major source of reptile and amphibian mortality during the winter.

Unlike Painted Turtles, Wood Turtles cannot survive oxygen deprivation even for brief periods and can only overwinter in streams where anoxic conditions are very rare.

The same ice that traps turtles underwater during the winter also creates a barrier that prevents gas exchange between the water and air. Many bodies of water steadily lose oxygen throughout the winter until becoming anoxic. At this point, turtles are unable to gather the oxygen required to sustain them through their skin through so-called “butt breathing”. To compensate for oxygen depletion, their metabolism drops further, to just 1% that of summer levels, and they start burning glycogen as an energy source. Burning glycogen from muscle tissue produces enough ATP to power the turtle’s cells, but also produces lactic acid as a byproduct. This same process is what causes muscle fatigue and soreness during exercise, but in turtles the lactic acid levels in their bodies steadily rise without reprieve during periods of anoxia and can eventually cause a condition called anoxic acidosis, and death. Different turtle species have different levels of tolerance to anoxia and the resulting acid buildup, and Painted Turtles top all other North American species. To balance out the lactic acid, Painted Turtles precipitate calcium and potassium from their skeleton and shell into their blood stream, which buffers the acidity and staves off symptoms of acidosis. That is not to say Painted Turtles are immune to problems caused by lactic buildup and indeed, many die after prolonged periods in anoxic conditions. Those that survive are lethargic for some time and can be seen hyperventilating after emergence in an attempt to get as much oxygen into their system as possible.

Prolonged oxygen deprivation is eventually lethal to all northern reptiles and amphibians, even Painted Turtles. Eastern Newts (Notophthalmus viridescens), for example, almost always overwinter underwater in the north and stick to aquatic habitats with minimal flow. While beaver ponds are an ideal habitat for Eastern Newts, those beaver ponds usually freeze completely over during the winter, trapping the newts under the ice. Like Painted Turtles, newts drastically lower their metabolisms and oxygen requirements in cold water to the point where they no longer need access to surface air. Anoxia, however, is more problematic to the newts than to Painted Turtles. While amphibians are capable of anaerobic respiration for short periods of time in cold temperatures, even for days in some cases, they do not have much bony material from which to buffer acidity caused by the buildup of lactic acid and are thus much more susceptible to its effects.

 

When wetlands become anoxic in winter, Eastern Newts seek out openings in the ice to access oxygen and on rare occasions can be seen in very large numbers.

I’m reminded of a case a few years back where a woman in Vermont found a small opening at the edge of a frozen beaver pond that was packed full of at least hundreds of newts, all clambering for access to the surface. Presumably the water in the pond had gone anoxic and every residing newt flocked to the one spot where they could access oxygen. While the fate of those newts is unknown, a friend of mine at another site found hundreds of newt carcasses piled together in one spot at the edge of a similar pond at the end of winter. Most likely that pond also became anoxic and the newts congregated at an opening near the edge. What exactly killed those newts is hard to say, but a refreezing event would have cut them off from their oxygen and may have resulted in their death. Reptiles and amphibians that overwinter underwater vary in their tolerance of anoxic conditions, but all have their limits.

Not every reptile and amphibian in the north can substantially supercool or survive being frozen, indeed most cannot, but that does not stop many species from pushing the limits. Jefferson Salamanders (Ambystoma jeffersonianum), for example, cannot freeze and can barely supercool, but they emerge from their overwintering sites below the frost line, migrate across or under snow to their breeding pools, lay their eggs, and then sometimes make it back to their upland habitat before Wood Frogs even emerge. Jefferson Salamanders have even been seen emerging through holes in the snow around the stems of small saplings and are sometimes seen breeding under layers of ice.

While Blue-spotted Salamanders cannot survive freezing like Wood Frogs and some other species, they emerge as soon as the ground starts to thaw and on rainy nights can often be seen moving across snow.

The sheer number of amphibians that emerge at the first signs of spring while there is still snow on the ground can be breathtaking. There is a site in central Vermont where the public is invited to help monitor migrating amphibians every spring on rainy nights. On many occasions at that site I’ve seen salamanders migrating over snow, and sometimes while it is actually snowing. You may read that temperatures need to be about 4C (40F) for major amphibian movement on rainy nights, but up north as long as air temperatures are above freezing and the ground is moderately wet those animals are good to go. One night we counted nearly 1000 Blue-spotted Salamanders (A. laterale) over the course of just a few hours, along with hundreds of other amphibians including Spotted Salamanders (A. maculatum), Four-toed Salamanders (Hemidactylium scutatum), Red-backed Salamanders (Plethodon cinereus), Wood Frogs, and Spring Peepers. Similar migrations uphill take place in the fall, but that uphill movement tends to be more spread out so the numbers on any one given night are not nearly as spectacular. The north might not have the high diversity of reptiles and amphibians as the south, but despite spending extensive time in both Georgia and Texas I have never witnessed such numbers in warmer climates.

Sometimes seen gathered in large breeding congregations, Common Gartersnakes emerge and mate early in the spring, even when there is still snow on the ground. Their ability to survive brief periods of body freezing may allow them to emerge from their hibernacula so early in the year.

Another extreme case of breathtaking numbers is the Narcisse snake pits of Manitoba. In places where foraging habitat is abundant, but overwintering habitat scarce, gartersnakes use communal dens and emerge in large numbers at the first signs of spring. In Narcisse, thousands upon thousands of the snakes emerge at the same time, slithering over top of one another in massive piles as part of a breeding frenzy, usually in April while there is still snow on the ground. To a much lesser extent, this is something I have seen in Vermont on a small island surrounded by swamp. The swamp is an excellent place for the snakes to forage, but seemingly every snake in the swamp migrates to a single rocky island to overwinter where they can get below the frost line, but remain above the water table. The island has a much warmer microclimate than surrounding areas and is one of the first places in the state to thaw, so getting to the island in time to see the snakes often means kayaking through narrow channels in the ice, sometimes even kayaking over the ice, then hiking through thick cedar swamp in chest waders to avoid getting soaking wet during the inevitable “post holing” events. I can think of more than one person who has told me to never bring them to the island again, but those who survive the journey are rewarded by a long-awaited taste of spring and can see dozens of snakes crossing patches of snow and curiously looking for mates. Interestingly, the snakes on that island are so single-mindedly focused on finding mates when they emerge that they will approach sources of vibration; I have found one way to attract the snakes is to just drop a log on the ground repeatedly in one place and within moments snakes start making their way toward me.

Accessing "snake island" early enough in the year to see the Gartersnake emergence can be tricky, and sometimes involves kayaking through narrow channels in the ice.

There are plenty of biodiversity hotspots where herpers flock to see the greatest number of species, but there are very few events that attract interest from outside the herpetological world to reptiles and amphibians apart from those events related to northern winters. The spring amphibian migrations draw people out into the cold wet weather who would otherwise never be caught outside in those conditions. Mudpuppy night attracts the occasional tour bus across international borders so people can spend a night wading out into fast-flowing water to see salamanders, getting covered in ice in the process. The spectacular snake pits of Manitoba attract tourists from around the world and are a major source of revenue to rural areas around Narcisse. A place called “Snake Road” in Illinois, where huge numbers of snakes can be seen migrating to and from their hibernacula, is almost considered sacred ground among the field herping community and people from around the world flock there to see the event for themselves. None of those spectacles would take place without an icy winter.

As a herpetologist from Vermont who has spent most of my life in the north, people often ask me why I wouldn’t rather live down south where there are more species and much longer field seasons. Truthfully, I’ve lived in the south, and while I am always excited to find new species, I spent a lot of my time down there reminiscing about kayaking over ice to witness the gartersnake emergence and searching for amphibians on cold rainy nights. Of course there are plenty of amphibians crossing roads in the rain down south, but not on such a large scale as I am used to. Not counting Mudpuppies, there isn’t much to see herp-wise up here for four or five months out of the year, but I wouldn’t trade the northern herping experience for anything and the incredible abundance of animals to be seen in the spring and fall more than makes up for their scarcity in the winter. The fact that there are complex biological mechanisms taking place under the surface to make it all possible just adds an extra layer of intrigue; the cake under the icing, so to speak.

Despite having less species to see than in warmer parts of the world, the winter ecology of reptiles and amphibians remains one of the most fascinating aspects of herpetology to me.

Acknowledgments: Special thanks to everybody who contributed photos for this article, especially Isaac Chellman, as well as to Dr. Kenneth Storey and Janet Storey, who not only provided photos of frozen frogs, but have contributed vast amounts of knowledge to the scientific community about the mechanisms animals use to survive freezing conditions. Visit http://kenstoreylab.com/ for more photos and information. Thanks also to Fred Schueler and Aleta Karstad for their continued service to the herpetological world by hosting Mudpuppy Night, an event I have greatly enjoyed participating in over the years.

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