Cold Tolerance in Small BirdsThis article was inspired whilst watching a Snowfinch in the icebox of a blizzard in the Italian Alps
The notice at the bottom of the chairlift proclaimed in quaint Italian-English "Attention! Heavy Wind in Height". It did not lie. At the top the water bottle in my backpack was solid ice, my scarf was frozen with the consistency of short-crust pastry and moulded to the contours of my face and Annie mentions that she canít feel her feet. Spin-drift snow is being whipped under the chairs as they turn the corner for the return journey, and there, happily mooching about, is a Snowfinch picking up interesting tit-bits dropped by lift passengers or deposited by the vortex with the drifting snow. Iím thinking "How can something so small survive these conditions that make us so cold?" and so a bit of web research is needed!
Wildlife living at high elevations must be able to cope with high winds and cold temperatures. Alpine songbirds face a particularly severe challenge because their small body size is directly exposed to the weather. Why is it worth any animal living in these conditions with such high energy costs?
The answer is because they can - there would otherwise be empty niches. In winter most alpine areas still have wind-swept ridges with exposed herbaceous stems and seeds for foraging, and as winter progresses towards spring vast numbers of cold-numbed insects are swept up from lower elevations to land on high elevation snow fields. These insects trapped on snowfields provide a nutritious and abundant food supply for alpine-breeding birds and other animals. Most alpine passerines are both granivorous and insectivorous to take advantage of these mixed food supplies.
But weíre interested in the cold. How do birds survive? The alpine environment is extreme but all birds that stay in residence in cold climates over winter need to maintain their body temperature. Birds, like mammals, are warm-blooded animals or endotherms. Their physiology and biochemistry has evolved to the state that it only works properly if the body is maintained at a relatively high and constant temperature. In birds this temperature is around 39-43 °C, which is some 2 degrees higher than mammals because of their need for a higher metabolic rate to sustain flight.
In fact, only the core of the body need be maintained at these temperatures. The extremities can be allowed to drop to lower temperatures without significant harm, and, indeed, some birds (and mammals) can allow their core temperature to drop significantly without harm in certain circumstances, e.g. hummingbirds can go into torpor whilst sleeping overnight.
To maintain a constant core temperature irrespective of the temperature of its surroundings, a bird must be able to control heat loss and heat production. These controls must be carefully balanced because the enzymes, those key biochemical components of living tissue, work best at temperatures just below those that will deform them and stop them from working, and yet the body produces a large amount of heat when a bird is active and the diurnal range temperature on the ground can be large - in alpine areas can be as much as 50 °C. The core temperature in birds and mammals is set at this optimum temperature for enzymes, so in fact the body is less tolerant of a rise in core temperature than it is of the equivalent drop in core temperature.
How is Heat Lost?Since the core temperature at around 40 °C is almost always higher than the ambient temperature of the birds environment, there is always a tendency for heat to be lost from the body. Four processes are involved:
The temperature of a bird is the balance of heat lost against that gained from the environment and that produced internally. So, it can maintain its body temperature in cold conditions by protecting against heat loss or increasing heat production.
Protection against Loss
More heat is lost by convection than by conduction when there is any significant air movement next to the skin. Thus the ability of the material covering the body to trap air and stop it from moving is more important than it being a poor conductor of heat. As it happens, air is also a very poor conductor of heat, so a trapped layer not only minimises convective loss but also reduces conductive loss. If the covering that traps the air is also a poor conductor of heat, you have the ideal insulating layer.
Here are estimates of conductivity for some key components:
Notice that air is the poorest conductor (best insulator), and that feathers and wool conduct 10 times less than cold skin and 30 times less than warm skin. (Bird skin is thinner than mammal skin and its conductivity may be somewhat different.) Wood, which we regard as a reasonable insulator, has about the same conductance as warm skin, and iron, which we know is a good conductor of heat, is some 3000 times poorer as an insulator than air. It is unlikely that a bird would choose to roost on the iron rail of a ski building even if it were sheltered from the wind!
A birdís body is defined by and covered with contour feathers. Beneath or amongst these to provide further insulation and to fill out its shape are semi-plume and down feathers. Contour feathers have a small downy portion at their base (closest to the skin); semi-plumes are virtually all downy; and down of course is all downy and completely lacks any interlocking barbs. The feathers are arranged in such a way that the outer part of the contour feathers provides a streamlined, sleek outer covering over a layer of air-trapping down. This arrangement provides excellent insulation, so long as the wind doesnít get behind the feathers. It also provides the bird with a great deal of control. Insulation can be increased by erecting the feathers to increase the amount of air that they trap or reduced by compressing them against the body, and if it is very hot then the feathers can be raised high enough to expose skin and allow the trapped air to escape thus maximising heat loss by convection. Longer term regulation of insulation can be achieved by increasing or decreasing the amount of down.
Water is a better conductor of heat than air by a factor of 22 (see table above), so birds must be very careful with their preening to ensure their feathers remain waterproof at all times. Water will quickly displace the air from feathers if they loose their proofing and this will place a bird in serious danger of death from chilling. Regular preening ensures that a bird is always waterproof. It keeps the contour feathers in the correct position with their veins properly knitted together as well as distributing the oily secretion from the Uropygial (or preening) glands at the base of the tail and powder from powder down feathers. Both of these substances are water repellent.
Some birds that live in cold climates have further specialised their body covering for insulation. Ptarmigans have heavily feathered, and thus highly insulated, feet. In this case the feathers, together with the toes, also function as snowshoes. Ravens living in the arctic have up to six times thicker, horny insulating soles on their feet than those that live in the tropics.
The colour and texture of feathers could also be used to increase radiative heat gain during the winter. Black absorbs (visible) radiation very efficiently whilst white reflects radiation efficiently. However, birds in alpine regions in winter are more likely to be white than black, indeed many moult to become white or whiter during winter. The main reason for this is almost certainly to reduce the danger of predation, since black birds on white snow are easy to see. Another reason may be that feather colour provides only very long-term, coarse control over temperature gain and there is a danger of overheating in sunshine (remember overheating is more dangerous than overcooling).
Birds can use behaviour to assist in thermoregulation, but only to the extent that it does not inhibit their primary activity - a bird cannot shelter or rest on one leg whilst at the same time foraging.
Un-feathered (un-insulated) body surfaces, the beak and legs, serve as important sites for heat exchange with the environment. By standing on one leg and tucking the other among its breast feathers, a bird reduces by one third to one half the amount of un-feathered area exposed. This is particularly important for birds with large legs and feet that rest in exposed situations - waders, ducks, geese, etc. By sitting down and thus covering both legs, heat loss from the limbs is minimized and overall loss is reduced by some 20-50%. Small birds will often sit for a while whilst foraging in cold weather.
Many birds sleep with their heads tucked under a wing and either sitting or standing on one leg. This is typical of waders who will also face the wind to prevent it from getting "under" their feathers.
Birds can also use behaviour to harvest environmental heat in cold weather by sun-bathing. Many small- and medium-sized species, especially passerines, assume sunning postures in which they squat or sit with their feathers slightly erected and wings drooped. And it seems to me that my bird-feeders are more often visited in the winter when they are in the sun, suggesting that in cold weather birds will forage in the sunshine whenever they can. Alpine birds have been observed to sit on dark rocks to warm up in cold sunny weather.
In bad weather and at night birds seek shelter, which can be limited in alpine areas. Tree "islands", especially when composed of conifers, provide good shelter and the clever bird will chose a spot on the leeward side when settling in for the nightís roost. Dwarf trees and shrubs provide good shelter if they have not been covered by snow. Crevices between rocks and in rock falls and the burrows of small animals (of which there are many judging by the amount of tracks one sees in the snow) are other options. Most species use snow roosts or snow burrows for sleeping or during storms. The Capercaille will actually make a burrow in deep snow.
Finally, a few species of birds actually huddle together at night. Wrens and tits, for example, are known to share holes and cavities and so many can pack themselves into such spots that those at the bottom have been known to suffocate.
Physiology and Anatomy
As we have seen the un-insulated legs of a bird are a potentially big site of heat loss, and where possible behaviour is used the limit this loss. Actually birds have evolved anatomical and physiological features to control heat loss from the legs and feet so that it can be minimised during cold winter weather (and maximised during the summer to prevent overheating). The arteries and veins of the leg are arranged to act as a counter current heat exchanger. They lie against each other so that heat in the arterial blood leaving the body core moves by conductance into the venal blood returning to the core from the cold extremities. Since the arteries and veins run in contact with each other for some length and, at any point, the arterial blood is always warmer than the venal blood, the heat exchange can be very efficient. This arrangement is more sophisticated in some birds than others.
In addition birds can constrict the blood vessels in their feet so that the actual volume of blood passing through is reduced, again minimising the potential for heat loss. Thus while the core temperature of a duck or gull standing on ice may be 40 °C, its feet may be only slightly above freezing.
A further physiological feature that has evolved in birds is the ability to maintain their body temperature at a somewhat lower level during periods of inactivity or in response to food deprivation. This is active regulation of a lower core temperature and it achieves significant energy savings for many species. It is more extreme in some species than others. For example, hummingbirds can allow their body temperature to drop by as much as 25-30 °C for several hours during the night or during spells of extreme weather. Of course there are costs in adopting this strategy, for example increased susceptibility to predation because of slower responses and a substantial metabolic cost incurred by arousal, but recent studies indicate that the ability to enter much shallower torpor for short periods may be quite widespread. Pigeons, for example, are known to have a lower nocturnal body temperature and to increase this by shivering (see below) just before dawn.
Body size is an important determinant of a birds ability to withstand the cold. As we have seen heat is lost from the bodyís surface. Heat is gained from internal biochemical activity which goes on throughout the body, so the bigger the body mass the more heat produced. As body size increases, surface area per unit of body mass (the surface/volume ratio) decreases - bigger animals loose heat more slowly than smaller animals. The lion looses heat 100 times more slowly than the flea. As size decreases it is increasingly difficult for an endotherm to maintain its core temperature by producing heat internally. The smallest endotherm is the bumblebee hummingbird at 2.2 g and this is pretty much the limit. Below this weight the metabolic rate required to offset heat loss becomes impossibly high.
Of course birds like other animals are largely stuck with the size of body evolution has given them. However, a study of alpine finches in the Himalaya showed that the heaviest species occupy the highest elevations.
Energy Budgets / Feeding
Astonishingly it is said to cost birds (and mammals) at least 90% of their total metabolism to regulate body temperature to maintain endothermy. The resting metabolism and energy required for regulation of body heat are higher in winter than in summer and, as we have seen, more energy is used per gram of body weight in smaller birds.
Judging from the weight of similarly sized British birds, the Snowfinch weighs about 50g. Coal Tits, a common resident of tree "islands" in alpine areas, weigh about 8g. Because the Basal Metabolic Rate (BMR - the minimum rate of metabolism, i.e. the rate of biochemical processes when an animal is at rest) consumes some 35-50% of the energy budget depending on the particular circumstances, small birds can only survive perhaps two days of enforced rest. A long lasting blizzard or prolonged deep frost that prevents feeding can take a significant toll of small birds.
The rule of thumb for calculating the amount of food required per day by a small bird is 30% of its body weight as dry weight of food (i.e. the weight of food after it has been dried to remove water). Of course different foods have different water contents, and birds eat a mixed diet. However, this rule of thumb means that birds weighing up to about 100g must eat approximately their own body weight in food per day to keep their energy budget in credit.
Although more energy is required to maintain endothermy in winter, this does not necessarily imply a much greater requirement for food intake, because birds change their behaviour, and also birds tend to value leanness to avoid predation over fatness to avoid starvation. Rough estimates tell us that foraging increases the BMR by 3.4 times, flying by 2.2 times and singing by 1.4 times. In summer, for example, a bird might spend 40% of its time singing. In winter birds are likely to spend less time singing and more time resting (enforced by longer nights), whilst the actual time foraging may be about the same (again because of day length).
Body heat is produced as a by-product of the biochemical reactions that drive normal body functions. Even when resting in a temperature neutral environment the actions of breathing, circulating blood, etc will produce heat. All functions are more or less efficient. "Normal" muscle contraction with the purpose of producing movement is only about 20% efficient. The remainder of the energy released by the biochemical reactions driving the contraction becomes heat. This heat is not necessarily wasted because it is first used to maintain the core body temperature. Only if too much heat is produced, e.g. during vigorous exercise, or at rest on a hot day, is it wasted.
When insufficient by-product heat is being produced to maintain core temperature, energy must be burnt with the specific purpose of producing heat. This is called thermogenesis and it has three requirements:
Two mechanisms for thermogenesis are known in warm-blooded animals - shivering and burning brown-fat. Only mammals have brown fat, so shivering is the only mechanism available to birds. Shivering satisfies the three requirements very well. Muscle tissue comprises a significant part of the body mass, it is wired up to the nervous system to enable fine control, it has a very large metabolic scope available in fine increments from resting to active and at least some muscle fibres are capable of sustained activity.
Since no external work is done in shivering, i.e. the animal does not use the energy produced to move around, all of the energy from the biochemical reactions is released as heat which is quickly distributed from the muscle tissue by the convective effect of circulation.
All birds shiver to produce heat. Actually the term shiver is rather misleading, because the opposing muscle contractions that result in the visible tremor that we think of as shivering do not necessarily need to result in any movement at all. For example, such contractions are also responsible for controlling normal posture. Because birds are wired differently to mammals they do not tremor when shivering. They probably benefit from this since the movement in visible shivering will increase convective heat loss, and small birds are known to be more cold resistant than small mammals.
Of course, all of the mechanisms available to an animal for regulating core temperature, not just the muscles used for shivering, must be coordinated and subject to fine control. The main centre of control is in the spinal cord in birds and an area of the brain called the hypothalamus in mammals.
Birds can acclimatise to seasonal changes in the environment by modifying their physiological settings, rather like adjusting a thermostat. Small birds have been found to increase their BMR and Summit Metabolic Rate (SMR - the maximum metabolic rate they can achieve in response to chilling) in winter. These and other aspects of acclimation, for example increasing the amount of down, have the effect of increasing cold tolerance, i.e. lowering the temperature at which they get hypothermia. In American Goldfinches living in Dakota, where the average summer and winter temperatures are approximately 20 °C and -6 °C, respectively, the BMR in birds in winter is 46% percent higher than that in summer, SMR is 31% higher and the cold tolerance level is -9.5 °C in winter birds compared with 1.3 °C in summer birds.
Much larger birds can adopt different acclimation strategies. Willow Ptarmigans, for example, are known to produce a denser coat of feathers and actually lower their BMR in the winter.
References and Further Reading