TORPID TURTLES UNDER ICE - Winter World: The Ingenuity of Animal Survival - Bernd Heinrich

Winter World: The Ingenuity of Animal Survival - Bernd Heinrich (2003)

TORPID TURTLES UNDER ICE

Snapping turtles are air-breathing reptiles that lay buried in the mud at the bottom of frozen-over ponds for six months of the year, without ever once coming up for air. Except to lay their eggs, these turtles rarely emerge from their watery world. I recall one I saw in Pease Pond near Dryden, Maine, when I was a kid fishing for perch. The turtle was as big as a washtub, and it was swimming slowly under our rowboat like some prehistoric monster. In my imagination then and memories now, it could well have been a plesiosaur.

There are snapping turtles in the beaver pond near my house in Vermont now. In early June the egg-laden females make their short migration up and out from the beaver bogs to their traditional nest sites. A by-now-familiar foot-long snapping turtle has chosen a sunlit patch of gravel alongside our neighbor’s driveway. In June she scoops out a cavity at that spot with her hind feet and deposits about a dozen white leathery eggs. Then, after covering them, she lumbers on back down to the bog. In early September the hatchlings dig to the surface, cross the road through the woods, and they too slip into the bog. There they bury themselves in the mud and remain until spring.

Turtles are measured in superlatives, from the Galapagos turtle that lives 150 years to the oceanic leatherback that weighs up to fifteen hundred pounds. Turtles have been around and have changed little since the Triassic ages of about 200 million years ago. They shared the earth with the dinosaurs for well over a hundred million years. They have adapted to deserts, oceans, and cold climates. To me they are the most interesting and attractive of reptiles, and I find baby turtles especially appealing. That even includes the baby snapping turtles, whose tails are longer than their bodies and who look like miniature alligators. Unlike the young of birds and mammals, turtles seem complete and self-sufficient replicas of the adults.

The common snapping turtle (Chelydra serpentina) can grow to be three feet long, snout to end of tail, and weigh up to fifty pounds. When they are out of the water, snappers live up to their name. They will lunge at you, and can reputedly snap a broomstick (probably an exaggeration). Still, you don’t mess with them. One early morning in September 2000, as I saw the first white frost on some of the grass and the purple New England asters were just starting to flower, feeding the migrating monarch butterflies coming by daily in droves, I heard a splashing down on the beaver pond. Geese? The splashing continued. A wading moose? I rushed down and peeked through the thick foliage. Mallards—about twenty of them—were flying around the pond in alarm, landing in scattered groups. No geese and no moose were in sight, but on the other side of the pond, close to shore, I saw a steady splashing-churning of the water. I studied this strange phenomenon through my binoculars, without getting any clues. I would have to get closer, so off I ran through the woods and through ankle-deep sedgy shallows, then onto the beaver dam where numerous deer had also crossed recently, judging by the fresh tracks in the new mud laid down by the beavers.

Once I got near the commotion, I saw that it was a duck helplessly flapping in place. I waded out through the muddy water beyond sedge hummocks, till I neared the duck. It flailed harder, dove and disappeared totally from my sight in the now quite muddy water, but reappeared in seconds. Finally I grabbed it, and it then ceased all movement. As I suspected, the duck was attached to something solid. A log? I lifted the duck a bit higher, exposing yellow-pinkish legs and feet. There, attached to one foot, was an object the size of a quart jar, coming to a triangle near the front. It was algae-covered—except for the eyes. The snapping turtle had a solid grip on the duck’s right foot.

Common snapping turtle.

I presume the duck was lured within striking range because the turtle’s back looked like a moss-covered rock for a convenient perch. Although this may not be the designated hunting strategy of a couch potato, it may approximate it. This turtle’s close relative, the alligator snapper (Macroclemys temmincki), clocking in at a record weight of two hundred pounds, is probably the ultimate low-energy investment hunting specialist. Lying on the bottom with its mouth open, this turtle just wiggles its pink, wormlike tongue and lures its unsuspecting prey directly into its mouth. Talk about efficiency.

I started walking backward toward the shore, pulling the duck with the turtle attached to its foot. The turtle would not let go. I looked into its hard yellow eye with its starred little black iris—the eye that had, scarcely unchanged, seen the dinosaurs come and go.

How could I get the turtle off? I wondered—because I was not going to let this creature finish drowning the duck. That might take hours in this shallow water. I had no weapon at hand, and contemplated slowly dragging the monster to shore and finding a stick to beat it over the head. Maybe it would then let go.

As I was thus slowly maneuvering the pair toward shore, the turtle finally obliged and let go. Now I held a duck, which still had not moved and had remained totally silent. The web between its toes was badly torn. But this injury would heal. I threw the duck into the air. It quacked a few times, and flew off.

Meanwhile the turtle slowly, ponderously, moved on the bottom out of the stirred mud into less murky water. I reached down and grabbed its long tail. I don’t know why. The engagement it had had with the duck was long enough. Ours somehow, wasn’t yet. But what to do? I lifted it—hefted it—but perhaps wisely not all the way out of the water, even if I could have, which wasn’t a sure thing. But I lifted it high enough to see its pale yellow underside—of thick neck and belly. What could I do? Nothing. I let it go—it resumed its slow lumbering journey away from the shore, toward deeper water. Perhaps I should have felt guilty—I may have deprived it of its last meal before it would fast for six months while stuck in the mud.

A year later, as the latest crop of baby common snapping turtles were digging themselves out of their nest in the gravel of my neighbor’s yard also to enter hibernation quarters in the pond, I scooped three of them up and put them into an aquarium along with minnows, whirligig (Gyrinid) water beetles, tadpoles, and one giant predaceous (Dytiscid) water beetle larva. The hatchlings seemed lively enough, but they refused all food. Instead, one became food: within a day the water beetle larva killed it by clamping its hollow pincers into the turtle’s neck and injecting digestive juices. I removed the predaceous beetle larva while it was sucking up its meal, and then left the aquarium outside.

By December the aquarium had acquired a thick layer of ice. The ice did not slow down the minnows or the beetles, which both remained as quick as before, but the turtles settled to the bottom and looked dead. I presumed that was normal, for a turtle. Finally in late December, I brought the aquarium inside and when I removed the remaining ice and pulled up the turtles, they still seemed stone-dead. However, as soon as they warmed up they became as lively as they’d been before. They were now likely smaller (lighter) since they had not yet eaten anything in the three months since hatching out. What had changed was that they were now voracious feeders, and they could only now start to grow.

Hibernating baby snapping turtle.

Perhaps hatchling snapping turtles don’t feed until after they have hibernated. If so, they are among the few creatures that normally start their life with an eight-month fast. At near 0°C, their metabolism shuts down and helps them conserve energy and/or reduce their need for oxygen. In contrast, northern fish compensate and adapt their metabolic machinery to be active despite the otherwise normally depressed metabolism due to low temperature. (Summer-active minnows that I put into ice water went belly up in seconds.) In fish, that temperature compensation involves activating new enzymes (isoenzymes) that perform the same function but that operate at lower temperatures where the previous enzymes would normally shut down.

A PROBLEM THE TURTLES and other winter water dwellers face that is closely related to food or energy supply, is oxygen supply. All turtles breathe air with lungs, but many species spend the entire winter without the opportunity to take a single breath of air, since they remain locked in under the ice. I have on rare occasions seen a turtle rowing along in slow motion just under the clear ice of an early October or November freeze-up. The turtles’ longest dives of the year are then just beginning, or may have already been in progress for a month. The duration of a turtle’s dive is determined by its ability to get oxygen from the environment and by its ability to accumulate an oxygen debt in its tissues. For dives of a winter duration in an air breather, that precludes engaging in vigorous, or almost any exercise, which snappers manage nicely.

The first sheet of clear transparent ice that covers the pond still allows sunlight to penetrate to the pond plants, and their photosynthesis still produces oxygen at low rates. The oxygen they give off dissolves in the water and is sealed in. As snow later covers the ice, less light penetrates to power the plants and their vegetative portions die. Now they start to rot, and to remove oxygen from the water.

Low water-temperature is an advantage to many organisms, because cold water absorbs and retains more oxygen than warm water. Most of the active water animals have gills to take in that oxygen. The aquatic insect larvae have them—dragonflies, damselflies, caddisflies, stoneflies, mayflies—as do the overwintering tadpoles of green frogs, bullfrogs, and some others. However, none of the few adult insects living underwater have gills, even those which are fully aquatic. That’s probably because the adults have only secondarily invaded the water, and their air-breathing mechanisms have continued with special adjustments added for life in the water. As adults, they were evolutionarily locked in to air-breathing.

Diving beetle adults and aquatic bugs carry air down with them. The predacious diving beetle Dytiscus, which captures tadpoles and small fish (and one of whose larvae killed my snapping turtle), carries a bubble of air hidden under its wing covers that it may expose to the water so that oxygen can diffuse in. Some other beetles, Hydrophilidae, and the back-swimming bug Notonecta, have their ventral body surface covered with a thin film of air (called a plastron) that shines silvery in the water. Like the Dytiscid’s air bubble, this air layer is connected to their air-using tracheal system, and oxygen used up from the air film attached to their bodies is replaced by oxygen from the water passively following the concentration gradient. As a result they can stay active even as ice covers the water.

The water under the ice provides an ideal environment for the animals that can breathe there. It is the one assured refuge from freezing, and many predators are excluded. For centuries it was presumed that birds spent the winter there. Not knowing much about bird biology and evolutionary constraints, it could long ago have seemed logical to observers that the swallows in the fall that skimmed closely over the water surface would spend the winter in the mud under the ice, since frogs, salamanders, and the myriad insects that emerge as adults from the water in the spring fly off and often live far from water. Of course, birds don’t hibernate in the mud, and it is not because an impossible physical hurdle stands in the way for evolution of such capacity. The major problem is probably evolutionary inertia. You can’t convert a jet plane to a prop plane, or vice versa. But what you can do is improve each, up to a point. As with the adult air-breathing insects, birds are historically locked into air-breathing. You can’t just make them water-breathing. And turtles?

Present-day turtles include the already-aquatic species that are evolutionarily predisposed or preadapted for life in the water. Even now, turtles are arguably the world’s best divers, and a winter’s hibernation under the ice is a prolonged dive—one that may extend to over six months of the year. Durations depend on the species and the physical characteristics of the specific hibernation site chosen.

In one study by Gordon R. Ultsch and colleagues (2000), map turtles (Graptemys geographica) were equipped with tracking tags emitting radio signals and found to range up and down the Lamoille River in Vermont and into Lake Champlain over at least a dozen kilometers. In the autumn as water temperatures drop quickly from 22°C in August to 11°C in September, and 2°C in November, the turtles congregate in one assembly about three kilometers up from the mouth of the river. This communal map turtle hibernaculum (which also includes softshell turtles, Apalone spinifera) was investigated by the biologists using scuba gear. They saw turtles pile on top of each other in a deep depression where there is negligible current. The turtles stay at the same site from November to the end of March. After the ice melts and when water temperatures warm up from 0.1° to 12°C, the turtles again leave and return to Lake Champlain for the summer (Graham et al. 2000).

After ice covers the Lamoille in December, the turtles are unable to come up for air for about five months. Do they experience stress of submersion? The biologists studying these turtles (Crocker et al. 2000) returned monthly to the communal hibernation site throughout the winter. Using a chain saw, Carlos Crocker (from balmy Alabama) cut a hole through the ice and then dove down and retrieved turtles and gathered environmental data such as water temperature and oxygen tensions. He sampled the turtles’ blood to measure acidity, lactate, and oxygen and carbon dioxide concentrations. The conclusion drawn from the data was that these large thick-shelled turtles remain essentially aerobic (oxygen-breathing) all winter long despite their inability to breathe with their lungs. They avoid the progressive acidosis that results from anaerobic metabolism, suffering no apparent diving stress because their low metabolic needs for oxygen are met despite inability to take a breath of air into the lungs for months. Their oxygen needs are low due both to their physical lethargy and their low body temperature that reduces resting metabolism. How they accomplish any oxygen uptake at all is not clear. However, the hibernating turtles rest with their heads and legs fully extended on the river bottom and may thus be exposing as much skin as possible to take up dissolved oxygen from the water.

Our best understanding of the hibernation dive physiology of turtles comes from the painted turtle, Chrysemys picta (Ultsch et al. 1999). This species, like other water-inhabiting species studied, also shows no apparent diving stress under simulated hibernation dives in the laboratory at 3°C in normal, i.e., unaerated water. That is, they show relatively little rise in lactic acid and also no change in blood glucose. These results indicate that gas exchange through the skin is sufficient in these turtles as well, at least if they lay on the pond bottom at near 3°C. However, these turtles normally hibernate by burying themselves in the mud, which is nearly devoid of oxygen so that they apparently even deprive themselves of breathing through the skin.

In order to find out how the turtles respond to oxygen lack, the researchers (Ultsch et al. 1999) brought them into the laboratory and sealed them into water bubbled with nitrogen gas to drive off all the dissolved oxygen. The almost totally oxygen-deprived turtles then survived for “only” about four months at 3°C. Their blood lactate increased steadily throughout the whole time of immersion. Blood pH declined from slightly basic 8.0 to near-lethal levels of 7.1. The acidification of the blood (to near-neutral pH) was compensated for in part by increases in concentrations of positive ions (magnesium, calcium, and potassium) that buffer the acidity.

Southern populations of these turtles reached near-lethal blood pH in only thirty days, while western ones required four to five times longer to reach the same lethal levels. Eastern populations were intermediate. Thus, hibernation dives are different from ordinary dives, and different populations of these turtles have adapted to withstand the specific magnitudes of the stresses that they encounter in the wild during their hibernations.

Young painted turtle.

As already mentioned, map turtles hibernate in depressions of the river bottom where warm flowing water in the spring from the river drainage could reliably signal the arrival of spring. In contrast, painted and snapping turtles inhabiting small ponds hibernate under mud in shallow stagnant pools close to shore (Ultsch and Lee 1983) even though it is stressful for them in that nearly oxygen-free environment. Ultsch and co-workers (1985) suggest these latter turtles choose the shallow water of stagnant ponds to hibernate in because of some as yet unknown advantage. Perhaps, because such water would heat up rapidly in the spring, it could provide the turtles their emergence cue and thus reduce the length of hibernation. Turtles have a relatively short season in the north to recoup energy losses, mate, grow, and lay and mature eggs. However, hibernation in shallow water that might promote getting an early start in the spring has a large drawback; predators such as raccoons could reach them there. Turtles therefore probably choose the physiologically more stressful burial in the anoxic mud because that behavior would reduce predation, especially in fall and early spring when the turtles are sluggish.

The ability of a turtle to buffer its blood with potassium and calcium ions, to reduce the acidity of lactic acid, contributes greatly to its winter survival under the ice. However, somehow this solution doesn’t quite capture the whole reality of an amazing, astounding feat. It does not account for a turtle’s just plain toughness and tenacity.

Turtles, both painted and snapping, often get run over by cars on the country road where I live as they travel to and from their nest sites. One warm June day when I stopped to pick up what I thought was a dead washtub-sized roadkill snapping turtle, perhaps one I’d met earlier in happier circumstances, I was left to ponder what life or death might be to a turtle. A dozen or so Ping-Pong-ball-sized round eggs were strewn all around this smashed turtle. As I touched its tail, the animal retracted its legs. Thinking the badly smashed turtle might perhaps still be alive, although I knew it could never recover, I wanted to put it out of its misery quickly. I maneuvered my pickup truck to run it over squarely. Another car came by just then and the driver, quite understandably, stared at me angrily. But the good and difficult deed was soon done nevertheless, and I dropped the turtle off with my ravens after chopping off its head (since the body still twitched). To my great surprise the birds had still not fed from it by the next day. As I pulled once again on the tail of the long-since-headless turtle, her legs contracted into the shattered remains of shell, as they must have if the ravens had pecked it.

What is death to a turtle? what is being alive? For six months it stays under ice water, buried in mud, where all breathing, movement, and presumably almost all heart activity stops. In spring it comes up, warms up, takes a few breaths, and resumes life where it had left off. It has done so for the perhaps 200 million years or so that its kind have prospered with little change. After the nineteen-mile-diameter asteriod struck the Yucatan Peninsula in Central America 64 million years ago and raised a dust cloud that caused the “global winter” that killed off the dinosaurs, they continued to live on as superbly successful and diverse animals to the present time. Only now, subjected to ecological effects from humans, are some populations endangered. Otherwise, they are still so well designed that they require little change. Maybe they survived that fateful global winter after the asteroid struck earth much like they now routinely survive a northern winter, by simplicity. They reduce their energy expenditure to extend their oxygen and energy reserves.