Why We Run: A Natural History - Bernd Heinrich (2002)

Chapter 7. How to Reduce an Insect’s Flight Endurance

Ask now the beasts, and they shall teach thee.

—JOB 12:7

Hunting for scientific discoveries is a game. It’s much like hunting for wild game. Proximally, both are done for the fun of it, and both ultimately yield practical results. The problem is that life’s thickets are incredibly dense, and you have little idea what is lurking in them. You may want to go after a big payoff, if one is there and you’re sufficiently gifted to identify and pursue it. But there is no guarantee you’ll find it. I presumed, to get a Ph.D., I’d have to discover something totally unthought of and amazing, perhaps equivalent to discovering DNA, deciphering the genetic code, or elucidating the control of mitochondrial growth. As I already mentioned, my efforts were frustrating. Furthermore, as at UMO, my own physical ability to move soon fell short as well. After being unable to get data from DNA and realizing I wasn’t cut out for spending the rest of my life at a molecular biology workbench, and needing a new direction, I developed weird arthritis pains in the hands, knees, and feet that put me on crutches for a half year. As at Maine, the physical incapacity gave more time to spend in the library; then I made research probes to examine various aspects of behavior and physiology in tiger beetles, honeybees, caterpillars, butterflies, and hawk moths, trying to discover something of sufficient fun, that is, something new and of intellectual value. I eventually focused on problems in exercise physiology and temperature regulation in hawk moths. This choice was fortuitous, because it led to much more than I could have imagined.

What might insects teach us? Insects are creatures so different from us that they could have evolved on another planet. They have no brain as we know it, but instead a series of variously sized clusters of neurons. They have no veins, no liver, no bones, no lungs, no kidneys, and a very much different set of hormones. Except for those desert cicada active in summer at midday, insects don’t sweat to dissipate heat. Their “skeleton” is on the outside, rather than inside. They have no hemoglobin because they do not use their blood to transport oxygen as we do. Instead, small tubes called tracheae lead directly from closable portholes along the outside into the cells, with no intervening circulatory system. Nevertheless, despite our huge physiological differences, they solve similar problems as we do and by a number of accounts they are the most successful animals of the planet.

I knew hawk (or sphinx) moths and their larvae fairly well, and George Bartholomew and Franz Engelmann, my thesis advisers at UCLA, alerted me to a previous publication that suggested that these large insects might regulate their body temperature in flight—that is, keep it stable regardless of differences in external temperature. Since they fly at night and cannot bask like lizards and butterflies do, it seemed to everyone that they did this trick metabolically. Nobody had a clue as to how they might do it or if they really did. The topic concerned exercise, and my data from the moths soon related to their flight endurance.

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Hawk moth while feeding

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Hawk moth pupa

Unlike butterflies and bees, foraging hawk moths are continuous fliers, which, like hummingbirds, hover and fly from flower to flower without landing on them. They are hot-bodied only just before and during flight. Unlike a hummingbird, after perching and coming to rest, a moth’s heat production stops instantaneously, and body temperature cools by passive convection to become essentially identical with air temperature within a minute or two.

Heat loss by convection into air is perhaps most easily explained with an analogy. Heat in the body convectively lost to the air is like dye leaking out of a cloth bag into water. The rate at which the dye diffuses into the water depends on the color gradient at the bag-water interface. Finally, when the color inside the bag equals that outside (that is, when the temperatures are the same), then all convection stops. If we place the permeable bag with dye (heat) into a fast-flowing stream (wind), the rate of dye loss (cooling) is greatly accelerated because the dye immediately adjacent to the bag is quickly removed, maintaining the color gradient. We do not, however, cool entirely passively. We actively shunt heat from the interior of our bodies to the skin, to maintain a higher than passively generated temperature gradient. We also sweat, which permits us to lose heat against a temperature gradient, that is, from a lower internal to a higher external temperature.

Like us, the moths need a high muscle temperature in order to exercise vigorously. When their environment is cool, they achieve that muscle temperature by a slowly accelerating exercise—by using their flight muscles for shivering prior to flight exercise. They do not, however, produce more heat in flight at lower than at higher air temperatures. Similarly, when we run at low air temperatures, we don’t use our leg muscles simultaneously to shiver. By running, we already increase our body metabolism from 1.5 kilocalories per minute up to 30, but we can’t shut the heat production off. It is an unavoidable by-product of heavy exercise even if we’re running on a hot day. Heat production and exercise are inexorably linked. We can reduce heat production only by slowing down, but this option is limited for a hawk moth, which needs to expend huge amounts of energy hovering in order to eat. In summary, heat production in the moths turned out to be strictly a by-product of energy expended for flying. Yet paradoxically, body temperature during flight remained stable within a remarkably wide range of air temperatures over which passive heat loss would vary widely. How could they keep their body temperature both high and stable in the face of a wide range of environmental temperatures where the rate of passive convection would be expected to vary hugely?

Not being able to reduce heat production when we begin to overheat while running, we instead sweat to get rid of extra heat. We can thereby keep on running and producing even more heat without overheating as long as we have enough fluids to sweat. I found no sweating in the moths, yet they still stabilized their body temperature. How they kept warm at low temperatures was clear, but how did they cool themselves at high temperatures? How do they get rid of extra heat to stabilize their muscle temperature in order to continue flight at high temperatures? To find out, I performed a series of experiments that proved they get rid of excess heat from the muscles in the thorax by a unique mechanism. They shunt the heat from the thorax into the normally cool abdomen using the blood as a heat-transfer vehicle. The abdomen has little insulation, so wind passing over it causes cooling by convection. This so-called convective cooling from the abdomen is comparable to the heat dissipated from our car radiator, after it is transferred from the engine by liquid coolant.

The moth’s abdominal heat radiator could keep the animal from overheating during continuous flight even at air temperatures of 30°C (86°F). However, I reduced my moths’ flight endurance to a mere two to three minutes by surgically doing the equivalent of crimping a car’s radiator hose—by tying off their heartlike structure that pumps blood. The operation destroyed the moths’ ability to transfer heat into the abdomen; thorax temperature shot up, while the abdomen stayed cool. The temperature of the muscles in the thorax that power the wings in altered moths rose explosively to the intolerable high temperature of 44–45°C (111–113°F), and like marathoners who run out of water for evaporative cooling, these animals dropped to the ground with heat prostration. I knew that the overheating, and not the incapacitation of their blood-pumping organ, was responsible for the moths’ limited flight endurance, because if the fur coat covering their flight engine, the thorax, was removed so that they could passively lose more heat, the altered moths flew well despite the heart operation. It may seem counterintuitive that the moths have a furry thorax, which helps keep in heat. Thick fur is indeed a liability during flight at high air temperatures, but it is useful at low temperatures, when the animals have the opposite problem.

I was surprised and pleased with these and related results and published five different papers, three of them in the prestigious journal Science. There soon came a flurry of other papers showing that exercise endurance in various mammals is also limited by overheating. Jackrabbits, red kangaroos, and cheetahs are all furred to keep warm, yet all were shown to overheat to the point that they had to stop running even in moderate heat. Humans, however, because of a superb sweating response, have remarkable running endurance in the heat.

The problem of sometimes having to stay hot to exercise, and at other times having to get rid of heat to continue to exercise, can also involve precisely synchronizing the breathing cycle with blood circulation. As I shall next explain, breathing causes blood to be pumped and heat to be dumped, and that gives some insects endurance in the heat.

To begin to establish the elegance of the insects’ solution, as discovered in bumblebees, we have to back up and review some basics of design. First, in bees the abdomen is attached to the thorax by only a tiny, narrow waist, the petiole. All of the heat that in flying bees is some hundreds of times above resting metabolism (the exact number depends on what body temperature is used to establish resting metabolism, to make comparisons) is generated by the flight muscles that pack the thorax. (In insects there are no muscles in the wings—all the muscles that power the wings are inside the body itself.) The abdomen’s temperature is generally close to air temperature, unless, as in moths, the abdomen is used as a heat radiator to get rid of excess heat from the thorax.

The flight muscles are totally aerobic; like distance runners, bees don’t go into anaerobic debt as sprinters do. Their large imageO2 max is made possible with the aid of air sacs in the abdomen. The whole abdomen pumps in and out as a piston, compressing and expanding the air sacs by positive and negative pressure. Those same pressure changes that pump air in and out of the thorax are also harnessed to help pump blood, and that blood either may or may not be used for heat transfer. When the blood is used to get rid of excess heat from the thoracic muscles, then the ventral diaphragm releases the hot blood into the abdomen in discrete pulses, while the cooler blood entering the thorax from the abdomen is also “chopped” into discrete pulses. The hot and cool pulses of blood bypass each other because they are shunted through the petiole alternately, in synchrony with the in-and-out abdominal breathing movements. I therefore dubbed this process “alternating” fluid flow to distinguish it from blood flow going simultaneously in opposite directions in adjacent vessels, called “countercurrent” flow.

When the bees are flying at low air temperatures or discontinuously (such as when working on flowers), they have the opposite problem, of needing to conserve heat in the thorax. Under this situation, blood flow between thorax and abdomen is much reduced, and breathing movements are no longer of importance for moving the blood. Instead, the heart fibrillates and passes a slow, thin stream of blood into the thorax. This mechanism allows recovery of heat back into the thorax that would otherwise be lost to the abdomen due to the countercurrent flow.

Physiological synchronization of different systems is now coming to be recognized for energy economy as well as temperature regulation. In running quadrupeds, especially in such energy-efficient distance runners such as dogs, there is a coupling of breathing with stride. The animal passively inhales as its front legs stretch forward, and it exhales as it pulls those legs back and the volume of the chest cavity is reduced. As a result, energy necessarily expended for striding reduces the amount of energy otherwise required additionally for the mechanics of breathing. Birds and many insects similarly harness the thoracic volume changes that automatically result from their limbs’ movement, to help pump air. We humans, in contrast, were thought not to have such coupling of breathing with locomotion, so that we must invest energy specifically to expand and contract our chest to breathe. However, I know that in myself there is a very distinct coupling of arm swings with breathing. It’s automatic, and hard to change. The coupling cannot save as much energy as it does in a flying bird or a running dog, or as much as the well-known bellow-type breathing of some insects in flight does, but it surely saves some energy on a long run.

Bumblebee Body Temperature Regulation by Blood Flow

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Heat Transfer to Abdomen (One Cycle of Alternating Current)

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Numerous Cycles of Alternating Current Flow

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What applies to moths, bees, and dogs appears to apply to exercise in many other animals as well, and I became increasingly aware of my own breathing, heart rate, sweating, energy stores, stride, and running pace. When I ran, I sometimes tried to visualize as many of these variables as possible, trying to “see” how they all worked together. When I became conscious of it, I realized that at normal ultrarunning cruising speed I maintained a very specific pattern of breathing to my steps. There were almost always three steps with each breathing cycle, two for the inspiration and one for the exhalation. When I took longer steps, the only difference was that the inhalation lasted longer. The synchronization was maintained even with changing effort. When I was striding very easily, it took me three steps to inhale, and when I was running up a steep hill, two. In all cases expiration took place in only one step, and inspiration coincided with the remaining steps. When not running, I could also monitor heartbeats, and one heartbeat corresponded with inspiration and the remaining heartbeats of the breathing cycle corresponded with expiration. I’m not sure what the significance of that rhythmicity is, but I suspect it has something to do with energy economy. According to David Costill, ultrarunners have 5 to 10 percent less energy expenditure than middle and sprint runners per given running speed, and such running efficiency may take years of training to develop; it costs a twelve-year-old runner 40 percent more energy to keep pace with a twenty-year-old.

Synchronicity felt right to me, and so I probably unconsciously fell into the rhythm, and at times I tried to become conscious of it to facilitate it. By almost explosively exhaling on the last step of the breathing-step cycle, I maximized the amount of time the lungs held fresh air. Like a pronghorn antelope, I keep my mouth open when I run. Undoubtedly this reduces the resistance of expelling air and thereby saves energy.

One can predict generalities of evolution, given common sense. But you can’t predict a bee’s mechanism of temperature regulation. The common honeybee, for example, turned out to be an extraordinary endurance athlete in hot, dry, desert conditions. It could fly, even at air temperatures near 40°C (104°F), close to its preferred body temperature. Convective heat loss works only if there is a steep gradient of temperature between body and air. Without such a gradient, it is possible to lose heat only by evaporative cooling. So, given the first datum, the second is generally a necessary implication. However, bees don’t sweat. This poses a quandary: What makes them special?

It turned out that they have a means of heat loss that is similar to one I saw used by rapidly overheating contestants on a race in over 80°F heat on the Bowdoin College track in Maine. Every couple of laps, the racers dunked their heads into a barrel of water the race director, Bill Gayton, had set thoughtfully alongside the track. The water evaporating from the contestants’ heads and backs kept them cooled and running despite the heat. Surprisingly, bees that have collected nectar have a variation of this approach. They regurgitate their stomach contents from the mouth and spread the liquid all over themselves with their forefeet. Once they are back in the hive, colony mates lick off the residual solids (sugar) that are left after the water has evaporated. However, relying on regurgitation for evaporative cooling is probably not a recommended option for us.

Some storks and vultures cool themselves by a reverse, yet similar, strategy. They defecate runny feces down their legs. The blood in the bird’s legs is cooled by the evaporation, which reduces overall body temperature by as much as 2°C. A turkey vulture sitting on a fence post in the sun on a hot day, calmly and deliberately defecating on its naked legs, is behaving in a way that makes sense. Anyone who has ever been running hard on a sweltering day will be able to identify with such behavior.

During my research with bees (later, at the University of California at Berkeley), I had corresponded with the world’s premier biologist of social insects, Edward O. Wilson at Harvard University, and I was pleasantly surprised to learn that he once also had the runner’s bug. Ed had aspired and now he inspired. Reviewing some of my running history, Ed declared out of the blue, “You could run a sub-2:30 marathon,” and I immediately wanted to show him right.

Committing to run a marathon was a snap decision. I read his letter, and bang—I knew I could not allow myself one possibility of an excuse or of second thoughts. I could not say, “I’ll start tomorrow.” So I jogged to the gym, changed up, and ran Strawberry Canyon. I had visions of finishing in the Boston Marathon and then walking up to Ed’s office at the Museum of Comparative Zoology seeing his broad smile as I’d scored one for our team, the one of biologists with butterfly nets and insect-killing jars.

Soon after I started training, I got a knee pain. I went to an orthopedic surgeon, who said, “You have (some sort of ) cartilage degeneration. If you don’t stop running, I’m going to have to take your kneecap off and throw it in the garbage can.” His exact words. They rang in my ears a long time. I figured, instead, that I had a loose piece of cartilage, which I could get rid of by grinding it down by running, so I increased my mileage.

Ed turned out to be right, the orthopedist wrong. A half year later I did almost what Ed predicted. But I didn’t bring him news. When I trotted up to his office, he’d already read the Boston paper, and he greeted me by calling out my finishing time: “Two twenty-five!” I’d run 5 minutes faster than he had predicted. This was something for both of us to enjoy. As is usually the case in science, you make a prediction, and if it comes out close, you are happy because you’re potentially right with one idea, and if it comes out different, you’re closer to some other idea that you didn’t even think of before. That’s even better.

During my training for the marathon, I had thought a lot about the exercise physiology of insects, especially that of my current subjects, the bumblebees, which I calculated on the basis of energetics to have a flight range roughly near my maximum running range, a marathon. But birds do much better.

Birds are a lot like us. They have roughly the same body plan, with the same organ systems. Like us, they have lungs, blood, true hearts, arteries and veins, liver, brain, and kidneys. They have the same basic types of limbs, sense organs, glands, hormones, and biochemistry. Their mechanisms of gas transport, immunity, development, excretion of wastes, and brain function are practically identical to ours. We differ from them mainly in how far and in what direction each of these common features has been stretched to serve specific adaptive scenarios. Birds are more highly evolved than we are regarding endurance physiology. They have achieved a true breakthrough in speed and endurance. Insects had revealed many secrets of endurance that relate to body temperature, but birds inform us about the ultimate endurance that is possible for flesh and blood.