The circulatory system plays a central role in thermoregulation by the moth, Manduca sexta

Have you ever gone outside on a cool fall or spring morning when few insects were active and yet met with bumblebees visiting flowers? Were you surprised? While you may have taken the meeting for granted, these early morning forays by bumblebees require some impressive physiology. Most insects use external sources of energy to heat their bodies, but there are some notable exceptions. Bumblebees maintain the temperature of their thoraxes, which house the flight muscles, at 30°C to 37°C regardless of air temperature (Heinrich 1979). Because they can warm their flight muscles, bumblebees can fly when environmental temperatures are as low as 0°C. A number of other insects use metabolic heat, Hm, to warm their flight muscles, including large nocturnal moths, which were the subject of some of the earliest studies of endothermic insects.  Bernd Heinrich (1993) has spent a great deal of his professional life studying thermoregulation by insects. Some of the inspiration that launched this work came to him when he was a graduate student recording the body temperatures of moths in the highlands of New Guinea. Heinrich relates how as he captured moths flying to a sheet illuminated by a lantern, air temperatures were about 9°C. Despite these low temperatures, some of the larger moths captured had thoracic temperatures of 46°C, 9°C higher than Heinrich's own body temperature. It was at this point that he became convinced that some insects can thermoregulate by endothermic means. However, you don't have to travel to the highlands of New Guinea to meet endothermic insects. Some of Heinrich's most elegant studies of thermoregulation have been done on moths from temperate latitudes.  Studies of temperature regulation by moths began in the early 1800s. Many of these studies were focused on moths of the family Sphingidae, the sphinx moths. Sphinx moths are convenient insects for study because many reach impressive sizes, large enough to be mistaken for hummingbirds. Heinrich's dissertation focused on thermoregulation by the sphinx moth Manduca sexta, whose large green caterpillars feed on a wide variety of plants including tobacco and tomato plants. M. sexta is among the larger sphinx moths and weighs 2 to 3 g—which is heavier than some hummingbirds and shrews, the smallest of the birds and mammals.  Since the nineteenth century, researchers have been aware that active sphinx moths have elevated thoracic temperatures. These early researchers also knew that temperature increases within the thorax were due to activity of the flight muscles contained within the thorax that vibrated the wings. Later researchers discovered that during flight, the muscles responsible for the upstroke of the wings and those responsible for the downstroke contracted sequentially. However, during preflight warm-up, the upstroke and downstroke muscles contracted nearly simultaneously. Consequently, the wings of a moth warming its flight muscles only vibrated. Once warmed up and actively flying, sphinx moths maintained a relatively constant thoracic temperature over a broad range of environmental temperatures. This was evidence that sphinx moths thermoregulate.  You can see that a lot was known before Heinrich began his dissertation research. However, a significant problem remained. No one knew how sphinx moths accomplished thermoregulation. Phillip Adams and James Heath (1964) proposed that the moths thermoregulate by changing their metabolic rate in response to changing environmental temperatures. In terms of our equation for thermoregulation, Adams and Heath proposed that the moths increased Hm when environmental temperatures fell and decreased Hm when environmental temperatures rose.  Several observations led Heinrich to propose an alternative hypothesis, however. He proposed that active sphinx moths have a fairly constant metabolic rate and so generate metabolic heat, Hm, at a constant rate. Heinrich also proposed that sphinx moths thermoregulate by changing their rates of heat loss to the environment. In terms of our equation for thermoregulation, the moths decrease their rate of cooling by convection and conduction when environmental temperatures fall and when temperatures rise, sphinx moths increase their cooling rates.  Heinrich tested his hypothesis with a series of pioneering experiments that demonstrated M. sexta cools its thorax by using its circulatory system to transport heat to the abdomen. In other words, the blood of these moths acts as a coolant. In his first experiment, he immobilized a moth and heated its thorax with a narrow beam of light while monitoring the temperature of the thorax and abdomen. Because it was narrow, the light beam increased radiative heat gain, Hr, of the thorax only. Heinrich used the beam to simulate metabolic heat production by the flight muscles. He observed that the thoracic temperature of these heated moths stabilized at about 44°C. Meanwhile, their abdominal temperatures gradually increased.  These results indicated that heat within the thorax was transferred to the abdomen. Heinrich proposed that blood flowing from the thorax to the abdomen was the means of heat transfer. To confirm this, he conducted a second experiment. He tied off blood flow to the thorax using a fine human hair. With this blood flow stopped, flying moths overheated and stopped flying. Instead of stabilizing at 44°C, the thoracic temperatures approached the lethal limit of 46°C. An interesting debate between two groups of researchers with competing hypotheses was decided by two decisive experiments.