HIBERNATING BIRDS - Winter World: The Ingenuity of Animal Survival - Bernd Heinrich

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

HIBERNATING BIRDS

The idea that birds hibernate started with a belief that the swallows that skim over the ponds in the fall spend the winter in the mud under the ice. After we learned about intercontinental migration, a more remarkable phenomenon, the first idea seemed so ridiculous that any mention even of hibernation in birds was automatically deemed nutty. Nevertheless, torpid birds were eventually found, and by highly reputable observers, including Nobel laureate Konrad Lorenz. When W. L. McAtee found a torpid, seemingly almost dead chimney swift, a normally migratory species, in mid-October 1902 (in Indiana), which quickly recovered in a warm room, he said: “That experience gave me an interest in avian torpidity and stimulated the collection of references on the subject” that he summarized. Among these references are accounts of torpid swifts and other “swallows” that were found in hollow trees, stovepipes, and rock crevices and clefts during the winter, after most of the population had disappeared. Most of these early accounts seem credible, aside from the likelihood that some of the “swallows” may have been swifts (since the terms were then often used interchangeably). However, in no case were the durations of torpor ascertained to see if the term “hibernation” was justified. All that is, except one set of observations made in North America fifty-five years ago on the poorwill, a bird I’ve met only in the literature.

The Birds of America (1917) is a large multiedited and handsome book illustrated with sketches, photographs, and 106 full-page paintings by the bird artist Louis Agassiz Fuertes, who went, I think, far beyond his famous predecessor John James Audubon in his handsome and lifelike bird paintings. I got it for a Christmas present when I was eleven years old from a neighbor, Mary Gilmore, who never knew how much joy she gave. It is, in my opinion, the best book of American birds ever produced, and its editor in chief, T. Gilbert Pearson, had this to say about the poorwill (Phalaenoptilus nuttallii, the western relative of the whippoorwill that I used to hear in Maine then):

Torpid poorwill (drawn from a photo in Jaeger).

“I first heard the song of the poor-will in a wild canyon in the mountains of New Mexico. In company with Charles F. Lumis, the archeologist, I was camping in the long-silent homes of the cliff dwellers, high up on the white tufa walls of the haunted cliffs of Tyuon-yi. It was a quiet summer night with the moon shining in great brilliancy. The surroundings were most impressive, and when the sudden cry of poor-will, poor-will, was borne on the air from across the canyon, it was as if a voice from the spirit-land had spoken.” He went on to say that this approximately seven-inch bird is strictly nocturnal, and like others of the Caprimulgidae, or “goat suckers,” it catches only flying insects. He presumed therefore, reasonably enough, that “these birds retire southward when winter appears.”

We gauge what we think is possible by what we know from experience, and our acceptance of scientific insights, in particular, is incremental, gained one experience at a time. Just as there was still much to experience about poorwills at the turn of the century, there is still much unknown about kinglets even now. One of those experiences that considerably stretched the physiological limits of what was thought possible for any bird after Pearson produced his book was an amazing revelation by Edmund C. Jaeger made in the winter of 1946-1947 in the Chuckwalla Mountains of California’s Colorado Desert (Jaeger 1948). The poorwill, which the Hopi Indians called the “sleeping one,” apparently hibernates rather than migrating. The Navajo are also familiar with the birds, and when Jaeger asked a Navajo boy whom he knew, “Where do they stay in the winter?” the boy answered, “Up in the rocks.”

Sure enough, on a granite ledge in a secluded crypt lay what appeared to be a dead poorwill. But appearances are often deceiving. After Jaeger picked up the bird, it stirred in his hand, came fully back to life, and flew away. The next year in late November 1947, Jaeger again found a comatose poorwill—maybe the same poorwill—back at the same spot. He checked on it at weekly intervals and it always appeared to be dead. But when he last visited it that winter, on February 22, 1948, the poorwill immediately flew out of his hand when it was removed from its place of hiding. According to Jaeger’s calculations, the bird was presumed to be in a comalike torpor for about eighty-five days, the time when there were no or very few flying insects in the Colorado Desert. On the evening of February 22, Jaeger first noticed many insects flying into his campfire and into the beams of his car headlights.

On the five mornings during the preceding eighty-five days, Jaeger had measured the bird’s internal temperature by inserting a thermo-probe into its cloaca. All his readings showed the bird’s internal temperature hovered near that of the air temperature, as is usually the case when an animal is dead. He could detect no heartbeat with an aid of a medical stethoscope and saw no breathing movements of the chest. No moisture collected on a cold mirror held in front of the bird’s nostrils. A flashlight shined a full minute into the bird’s right eye (which was almost completely open) failed to elicit any response whatsoever. Jaeger concluded: “I take it as evidence that the bird was in an exceedingly low state of metabolism, akin, if not actually identical with hibernation, as seen in mammals” (Jaeger 1949, p. 106).

To determine whether the bird returned every winter to the same spot, Jaeger banded it with a U.S. Fish and Wildlife Service aluminum cuff. To his great satisfaction, the bird returned to its hibernaculum on the granite cliff in the winter of 1948-1949. It survived a severe November storm of sleet and hail that left a layer of ice on the ground for a day afterward and air temperatures that remained near 0°C.

Given what the Hopi and Navajo knew already, we can’t say without qualification that Jaeger was making a discovery. But his reports surprised physiological ecologists perhaps as much as if he had verified the old fable that swallows hibernate in the mud. Jaeger’s two papers begat a flurry of lab studies: fifteen laboratory studies of the poorwill and related species have since appeared in the scientific literature. These reports extend, and perhaps require some reinterpretation (but not much) of, Jaeger’s original paper. They confirmed that the poorwill’s body temperature in torpor indeed becomes essentially identical with air temperature (Howell and Bartholomew 1959). The torpid birds can spontaneously arouse from body and air temperatures as low as 6°C, although when doing so the process can take several hours (Ligon 1970). At such low air temperatures, however, the physiological capability of arousing is seldom used (Howell and Bartholomew 1959), presumably because it costs the bird too much time and energy (and probably also because it brings them little since there are then no flying insects to catch).

The poorwill, although unable to arouse from temperatures near 0°C, can nevertheless survive such low body or air temperatures (Ligon 1970). Thus, there is no problem explaining the survival of the particular bird Jaeger observed in an ice storm at temperatures at or below 0°C. But I doubt that his birds spent eighty-five days in continuous torpor. Captive poorwills regularly enter torpor at night, but don’t remain in that state for more than four days at a time (Marshall 1955). Since Jaeger always measured body temperature of his bird between 10:20 A.M. and 11:30 A.M., it seems not unlikely to me that his poorwill could have warmed up to forage on some warm nights, to then return to its same perch and resume torpor by the next morning. Other caprimulgids, like the nighthawk, which is migratory, are much more reluctant to become torpid at night (Lasiewski and Dawson 1964), probably because they escape cold weather instead.

As would be revealed in the avalanche of studies following Jaeger, such patterns as those in the poorwill are only a slight modification on those later documented in innumerable other birds. The main feature that makes the poorwill remarkable is that it sometimes stays torpid for days at a time without rewarming, thereby showing that physiologically there is no distinction between hibernation and daily torpor.

THE SMALLER THE SIZE, the greater the physical tendency for rapid cooling and the greater the energetic advantage to staying cool. A turkey-sized animal is not likely to let itself become cold enough for torpor at night, but the smallest birds and mammals, weighing as little as about 3 grams, including hummingbirds, some bats, and some mice and endothermic insects, do so routinely, actively, and as an adaptive response. They are the daily hibernators. By stopping to shiver at the cessation of daily (or nightly) activity bouts, some may cool down to ambient temperature in minutes. They may then be picked up and seem dead or dying, and one often assumes such. However, when ready to resume activity a half day (or night) later, they shiver and heat up explosively. In minutes they are as active as before. Small perching birds weighing more than 50 grams do not generally go fully torpid at night, but they save at least some energy by reducing body temperature a few degrees Celsius.

The torpor option for conserving energy was little known until the 1950s, when Jon Steen (1958) in Norway examined the metabolism of titmice and five species of common finches captured one winter just outside his lab near Oslo. At night the birds reduced their heat loss by balling up—tucking their heads into their back feathers—but they also reduced heat production by lowered body temperature at night. However, when plenty of food was available, the birds maintained normal body temperature at night, shivering often the whole time, while sound asleep.

Torpor of one degree or another is a well-known strategy for conserving energy of many of our winter birds. No bird in North America has been as well studied in that regard, and is as familiar to many people, as is the black-capped chickadee (Parus atricapillus). This 10-to 12-gram bird takes sunflower seeds from bird feeders all winter, and no walk in the snow-filled winter woods is complete without at least one run-in with a family flock of these small, tame, and inquisitive birds as they search for food. Day in, day out they are active, no matter how cold the weather. In Alaska the birds show a peak of food-hoarding activity in November (Kessel 1976), similar to other tits (Nakamura and Wako 1988). Nevertheless, how they maintain an energy balance during long cold night fasts was a mystery until they were investigated in the early 1970s by Susan Budd Chaplin at Cornell University.

Chaplin’s study of chickadees in the Cayuga Lake Basin in New York focused on the most critical time for cold survival: winter nights. She began by determining energy expenditure of the birds as they regulated their normal day-active body temperature of 42°C at air temperatures as low as 0°C and as high as 30°C. She recorded the chickadees’ rates of energy expenditure (oxygen consumption) when they were placed into constant temperature in a sealed chamber in the lab. As in all other homeotherms (animals that regulate a high and constant body temperature), metabolic rates were predictably high at low air temperatures, to make up for increased rates of heat loss. Given the hours of darkness per night, Chaplin could calculate how many calories of energy reserves a bird might require to enable it to remain fully heated over the duration of a night, and then she compared to see how that number correlated with the calories stored in the body’s fat reserves.

Fat has more than twice the caloric content per unit weight as carbohydrates (such as sugar and glycogen). Fat is therefore the fuel of choice for long-distance travel and for other long durations of exercise, such as all-night nocturnal shivering of sleeping birds (Marsh and Dawson 1982). The chickadees’ fat reserves were determined by collecting birds in the woods (by shotgun) in the evening and again in the early morning, then chemically extracting their fat contents to see how much energy they used during the night. Body fat in the evening measured 7 percent and only 3 percent in the early morning. That is, the birds fattened up throughout the day and then burned off their fat to produce heat to keep warm during the night. Winter birds had higher metabolism (Rising and Hudson 1974) and generally maintained twice the fat content of fall and spring birds. Indeed, the ability in any birds to put on body fat in significant amounts is generally restricted to only those that need it for migration or surviving cold while experiencing food shortages. Birds with a dependable food supply and resident in a moderate climate show little or no fattening (Blem 1975), presumably because there are costs of being fat; it is better for them to be lean unless there are compelling reasons to the contrary.

Given Susan Chaplin’s figures, chickadees are already close to an energy edge at 0°C, far from the lowest temperatures they might encounter during any winter night. Unlike some seed-eating birds, who usually have more food calories available and who put on a lot more fat overnight (Reinertsen and Haftorn 1986), Chaplin’s chickadees did not have sufficient caloric reserves in fat to make it through a night at 0°C, if they continued to regulate the same body temperature at night as during the day. However, she discovered that, unlike the seed-eaters, they stretched their fat reserves by lowering their body temperature to 30° from 32°C, that is, to 10° to 12°C below the 42°C of normally regulated daytime body temperature. This readjustment of their body temperature set-point was sufficient to make their fat reserves last the night, despite vigorous shivering during most of the time they were sound asleep. Nevertheless, even with the caloric savings derived from hypothermia, the chickadees’ fat reserves in the morning were insufficient to last them through another day and night, such as could occur during a severe blizzard. To survive such commonly occurring emergencies or temperatures much lower than 0°C would require them to have special shelter at night where air temperatures are higher and convective cooling minimized and considerable energy would be saved (Buttemer et al. 1987).

Chickadees do not build winter sleeping shelters, but like other Paridae they show great flexibility in choice of roost sites for overnighting (Perrins 1976; Pitts 1976). Black-capped chickadees may sleep in almost any tight cranny or cavity (as can sometimes be deduced from their bent tail feathers in the morning); in dense vegetation such as vines; in conifers; and possibly in snow. Siberian tits have even been reported to dig 8-inch-long tunnels into the snow for overnighting (Zonov 1967). Although black-capped chickadees have not been reported to huddle at night or dig into snow, many of their relatives do (Smith 1991, p. 246).

Chickadee fluffing its feathers on a cold winter day. Tail feathers are bent from overnighting in cramped quarters to escape cold. (Drawn from photograph by David G. Aden.)

One of the chickadees’ remarkable winter adaptations is their plumage, which is denser than that of other birds their size (Chaplin 1982; Hill, Beaver, and Veghte 1980). Heat loss is mainly from the area around the eye and bill, and when the birds fluff out and then ball up to sleep, they are reducing specifically that area of heat loss by tucking their heads under their scapular (shoulder) feathers of the wing.

The fact that chickadees were cutting it close, though, even at modest winter air temperatures, only deepens the mystery of how golden-crowned kinglets survive. They are half the body size of chickadees and experience at some times double the temperature extremes of Chapin’s study birds. Do kinglets overnight without much larger fat reserves?

Charles R. Blem and John F. Pagels from Virginia Commonwealth University have provided the only data to help answer that question. In January-February 1983 they collected (shot) kinglets in Virginia throughout the day. Like the chickadees, the diminutive golden-crowned kinglets increased their fat stores during the day, from about 0.25 gram at 8 A.M. to about 0.60 gram at 5 P.M. Despite the kinglets weighing only half as much as the chickadees, these amounts of fat are nearly the same in absolute terms as the chickadees’. Thus, relative to body size, the kinglets put on twice as much fat per day as the chickadees. Nevertheless, even these fat reserves already seem low at modest air temperatures of 0°C for the northern winter nights of fifteen hours; Blem and Pagels calculated that a kinglet in such conditions would require approximately twice the calories contained in their maximum fat reserves to last the night, if they regulated their day-active body temperatures. The mystery of how they manage was not, and still is not, answered. Reductions in body temperature are likely although the one study that examined this possibility (in captive birds) found no hypothermia. I suspect that in the wild, at -30°C, and in fifteen-hour nights, they must become hypothermic.

The relevant question is how hyperthermic? No body temperature measurements of kinglets in the wild under severe (or any) winter conditions (such as -30°C and wind) are available, so we have no definite answer. The birds would predictably have a great and most urgent need of hypothermia for energetic economy at -30°C, but such regularly encountered temperatures would pose a great risk of freezing to death in birds that become too hypothermic. Birds that get too cold could become unable to respond. Not being able to shiver they might then quickly turn to ice; cooling down risks losing physiological control for being able to generate heat. The trick is to be able, like the arctic ground squirrels, to achieve a physiological state that is technically close to death, while retaining the ability to respond and come back to life on demand. Minihibernation overnight is a good strategy, but only if temperatures in the morning are high enough to allow the animal to passively heat up to the point where shivering is again possible and the bird is able to warm up quickly. Endothermic insects face the same problems as small endothermic vertebrates, but more acutely.

Consider, for example, the tomato sphinx moth (Manduca sexta), whose large familiar green larvae feed on tomato and other solanaceous plants. The nocturnal adult regulates nearly the same body temperature as does a hummingbird while in flight. After flight at, say 15°C, the moth immediately cools and within a minute or two it is torpid. In the evening, if air temperature is 30°C, it needs to shiver for less than a minute to be flight-ready again. But if air temperature is 15°C it must shiver for several minutes. If air temperature is only 5°C lower, however, then the animal is incapable of warming up at all. It would remain in torpor and assuredly freeze to death if temperatures were then lowered to below 0°C. Normally, however, summer-active moths are never subjected to such low temperatures, so they need no defense mechanism to escape death by freezing. Similarly, bats can afford to enter hypothermia to save energy, when they are within the safety net of a cool but not too cold cave. They can slip into torpor, secure that they won’t turn into a block of ice, as long as they overwinter in deep caves where temperatures don’t go below the freezing point of their tissues.

The owlet moths of the subfamily Cuculiinae that are common in New England, face the brunt of the problem of potential lethal freezing. To escape predators (bats) they are active in the winter. Their flight muscles are amazingly cold-tolerant, and they can shiver and warm up even from temperatures as low as 0°C, but they will freeze solid at near -10°C. Nevertheless, they don’t shiver to prevent themselves from cooling to lethal temperatures when subjected to temperatures approaching 0°C. Instead they seek refuge under insulating leaves and snow to avoid getting that cold. Neither the moths nor most ground squirrels, except arctic ground squirrels, are in any real danger because in the microhabitat where they hibernate they are sequestered from very low temperatures and so no alarm response to dangerously low body temperature has evolved in them. In general, few birds find secure shelter from the cold such as that afforded by deep caves or underground burrows. Winter birds may face temperature drops of from well above freezing to -30°C or colder over the course of a single night, and they simply can’t afford to relinquish body temperature control. Ironically, hummingbirds provide a conspicuous model of an adaptive response that applies to many birds in winter.

One of the noctuid winter moths at rest on a beech twig.

Nocturnal hypothermia is common in hummingbirds because of their small size, although if energy supplies are available and temperatures are not too low, the birds don’t have to resort to this option. In the black-chinned Archilochus alexandri and the Rivoli’s Eugenes fulgens, torpor is used only in an energy emergency (Hainsworth, Collins, and Wolf 1977). Similarly, in the broad-tailed hummingbird (Selasphorus platycercus), which successfully rears its young in the energetically near-marginal conditions of the Rocky Mountains, can go torpid even when incubating on the nest if energy crises result from rainstorms and low nighttime temperatures. In other hummingbirds, torpor occurs even in very fat birds. For them it serves as a mechanism to conserve their energy resources needed for migration (Carpenter and Hixon 1988). The Anna hummingbird (Calypte anna) found from northern California to Baja California, regulates its daily energy budget less by nocturnal torpor than by daily gain of energy stores, increasing its body mass by over 16 percent during the course of the day.

There is obvious benefit of torpor, provided the risk of losing physiological control in an environment where temperatures dip too low, is not too great. Some hummingbirds are unable to respond to lowering temperature by shivering if they cool down to 20°C (Withers 1977). These are species (Calypte anna and Selasphorus sasin) living where they don’t encounter temperatures lower than 20°C (southern California). Others, from colder mountain environments, regulate not only a high body temperature when active but also a low one when in torpor (Wolf and Hainsworth 1972). Two other hummingbird species (Panterpe insignis and Eugenes fulgens), from the high cool mountains of Costa Rica and western Panama, not only regulate but are capable of spontaneous arousal from body temperatures of as low as 10° to 12°C. As already mentioned, the arctic ground squirrel, a hibernator, was later shown to do the same at even much more impressively low temperatures. Some hamsters (Lyman 1948) and pocket mice (Tucker 1965) have also been observed to first allow themselves to become torpid but then retain the ability to resist cooling below a specific, much lower body temperature threshold.

One cannot predict what golden-crowned kinglets do in any specific area and under specific conditions. All we can be reasonably sure of is that they likely engage in some torpor, but very deep torpor is probably not an option. A kinglet in a windy winter night at -30°C would have to remain ever-alert. If it should stop shivering for several minutes, it would quickly freeze as solid as a teaspoon full of water.

There is, of course, a way out of the kinglet’s quandary, and that is to find a microenvironment, such as a verdin’s nest stuffed full of body warmers. However, such options are limited in the north woods. This habitat contains neither verdins nor birds who build nests like them. Kinglets are too large to burrow unnoticed into the feathers of an owl, as do hippoboscine flies in winter (and summer). And they are too small and frail to burrow into the subnivian zone under the snow like grouse do. They obviously can’t avoid freezing to death by diving under ice-crusted waters. And yet I’ve seen dippers (relatives of wrens) in midwinter in Yellowstone Park jump into the icy swift water of the Lamar River, disappear from view, and later pop up along the edge of the ice.

I’m not implying that I think even for one second that dippers, or kinglets, can stay down and hide in some crevice under the bank like a frog or a trout. There are lots of obvious reasons why they don’t, but why couldn’t they have evolved that ability? Much that animals have evolved to do would have seemed impossible to us, if experience had not taught us otherwise. And few inhabitants of the winter world have evolved more ingeniously, more bizarrely even, than turtles, frogs, and insects.