It is now mid-winter in the Northern Hemisphere. Skeletal branches frame the skyline, bees are holed up in their hives, birds mob feeders, and squirrels are conspicuously absent at the feeders they had monopolized all summer long. We shiver as we walk the dog who is dejected with no rabbits around to chase. How do animals like earthworms, insects, fish, frogs, reptiles, birds and squirrels endure cold winters? Still sticking to the theme of “Endless Forms Most Beautiful”, I will look at the lifestyle and metabolic adjustments that animals make to survive the cold.
Animals are built differently with different body coverings and metabolic processes. Fur, blubber, and down feathers are well known insulators. Hibernation is a well-known coping mechanism, but there are others. Animals survive by freezing and dehydration, brumation and torpor, by slowing circulation, by shivering, and by burrowing into decomposing matter. Some animals metabolize like cancer cells. Endless forms it certainly is. I’ll look at these mechanisms briefly before examining bees’ overwintering in more detail.
Many animals are limited in their abilities to escape to warmer climes, and their strategies for surviving freezing temperatures is to themselves freeze, or to avoid getting frozen by some biochemical or behavioral adaptations. Freezing causes the production of ice crystals which can damage delicate cells and organelles. Even so, many invertebrates, amphibians and reptiles allow the freezing of the extracellular fluids, with only the actual cellular contents protected from freezing with the production of antifreeze-like chemicals. Examples of these are many insects, intertidal species like snails and bivalves, some species of terrestrial frogs, reptiles such as the box turtle, some snakes and lizards [1]. Many familiar animals avoid freezing by dehydrating, hibernating, torpor, brumation and shivering. The mechanism of dehydration mirrors drought tolerance, where the animal loses water. Solutions with very high solute concentrations are more resistant to freezing, a property we use when we salt roads to prevent ice formation. Physical protections such as the cocoons of earthworm and spider eggs also help with freeze avoidance. Many animals depress their body temperatures and slow down their physiology either long term in hibernation or the reptilian equivalent called brumation. The difference is that hibernation causes the animal to be dormant and go without eating or drinking for prolonged periods, whereas brumating reptiles occasionally “wake up” to drink water. Both require metabolic and physiological slowing. Hibernating and brumating animals usually seek out places like burrows and caves where they will stay until the weather warms. Some animals such as bears become hyperphagic in the Fall to prepare, eating excessively to store food as fat in the body for use over the hibernating period. By contrast, torpor is a short-lived event, often lasting just overnight or a few days, and is seen in skunks, squirrels, and bees.
Bees slow down their operations in the late Fall. The queen stops laying and there is no brood left. Long-lived winter worker bees have replaced short-lived summer bees, and the drones are long gone. In a wintering cluster, bees seek to both prevent heat loss, and to produce heat. To prevent heat loss, bees cluster tightly. Individual bees have bifurcated thoracic hairs that resemble bird down and traps heat. The clustering of bees further closes ventilation passages to retain heat but also restricts the movement of oxygen into the center of the cluster, and this will become significant later on. As the temperature cools further, the bees draw into a tighter ball which allows them to generate and share body heat [2].
Regarding heat production, bees have two metabolic states, endothermy and ectothermy. In ectothermy, bees depress their temperatures, metabolic rate and heating capacity, going into a kind of torpor where they do not move much. Endothermic bees actively shiver their thoracic muscles to generate heat, an activity that requires high metabolic activity and oxygen use. Thermal imaging has shown that the center of the cluster is warm with temperatures averaging around 70oF (21.3oC) and a cooler periphery with temperatures of about 52oF (11oC).
But this begs two questions: 1. How do the ectothermic bees at the periphery produce even the small amount of heat that keeps them from freezing? 2. With bees packed so tightly in their cluster, how can oxygen even get to the center of a big cluster to power heat producing metabolic activity such as shivering? Producing that much heat by shivering requires oxygen, and water is produced as a by-product. Water production is surely a problem, because water can chill the bees if it is allowed to accumulate in the center of the cluster.
To answer question 1: Although it has not been directly demonstrated in peripheral bees, I surmise that ectothermy uses the anaerobic Warburg pathway which breaks down for survival at low temperatures [3]. The Warburg mechanism is a fermentation pathway that breaks down sugars in the absence of oxygen producing small amounts of energy. An astonishing recent discovery is that colonial naked mole rats survive without oxygen for an amazing 18 minutes using fructose by the Warburg method [4]. Bees have access to fructose and the genes for the Warburg pathway. For example, Africanized bees downregulate oxygen-based metabolism and switch to the Warburg pathway when they are aroused by alarm pheromone [5].
Endothermic bees in the core of the cluster bees use aerobic respiration, but the thorny question 2 is how the tightly packed cluster gets enough oxygen. Thermal imaging analysis of the movement of core endothermic bees over 21 hours of recording showed that bees appeared at the mantle surface at a rate of 6-80 bees/hour. This means that adult worker bees that show this endothermic heat production cycle to the surface and return to the core after lingering at the cluster surface between 10 seconds and 3 minutes [2]. These selected bees presumably travel between the oxygen-depleted core and oxygen-rich periphery, breathing deeply and then rushing to the center to shiver out some heat, over and over. The water released by endothermic bees still poses a problem, but some water will be needed by bees to stay hydrated. Significantly, the authors of this report [2] go on to say, “We conclude that visiting the surface by endothermic bees is part of the natural behavior in winter clusters.”
Bingo.
1. Storey, K.B. and J.M. Storey, Natural freezing survival in animals. Annual Review of Ecology and Systematics, 1996. 27(1): p. 365-386.
2. Stabentheiner, A., et al., Endothermic heat production in honeybee winter clusters. Journal of Experimental Biology, 2003. 206(2): p. 353-358.
3. Vander Heiden, M.G., L.C. Cantley, and C.B. Thompson, Understanding the Warburg effect: the metabolic requirements of cell proliferation. science, 2009. 324(5930): p. 1029-1033.
4. Park, T.J., et al., Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat. Science, 2017. 356(6335): p. 307-311.
5. Barros, L.F., J. Sierralta, and B. Weber, How doth the little busy bee: unexpected metabolism. Trends in neurosciences, 2015. 38(1): p. 1-2.
