Chapter 4 Temperature Relations

Aquatic Birds and Mammals

Now let's turn to thermoregulation by aquatic endotherms, where the aquatic environment limits the possible ways organisms can regulate their body temperatures. Why is that? First, as we have seen, the capacity of water to absorb heat energy without changing temperature is about 3,000 times that of air. Second, conductive and convective heat losses to water are much more rapid than to air, over 20 times faster in still water and up to 100 times faster in moving water Thus, the aquatic organism is surrounded by a vast heat sink. The potential for heat loss to this heat sink is very great, particularly for gill-breathing species that must expose a large respiratory surface in order to extract sufficient oxygen from water. In the face of these environmental difficulties, only a few aquatic species are truly endothermic.

Aquatic birds and mammals, such as penguins, seals, and whales, can be endothermic in an aquatic environment for two major reasons: First, they are all air breathers and do not expose a large respiratory surface to the surrounding water. Second, many endothermic aquatic animals, including penguins, seals, and whales, are well insulated from the heat-sapping external environment by a thick layer of fat while others, such as the sea otter, are insulated by a layer of fur that traps air The parts of these animals that are not well insulated, principally appendages, are outfitted with countercurrent heat exchangers, vascular structures that reduce the rate of heat loss to the surrounding aquatic environment. Figure 4.22 diagrams the structure and functioning of a countercurrent heat exchanger in the flipper of a dolphin.

FIGURE 4.22 Countercurrent heat exchange in dolphin ftippers.

Heat exchangers are so efficient at conserving heat that some species of fish are able to maintain a significant thermal gradient between some of their muscles and the external environment. While not capable of regulating the temperature of their body core, as aquatic birds and mammals do, these fish can selectively heat certain muscle groups and per- haps increase their swimming performance over a larger range of temperatures as a consequence.

Warming the Swimming Muscles of Large Marine Fish

Francis Carey (1973) was fascinated to learn that some fishes, such as tuna and mackerel sharks, have body temperatures above that of the surrounding water, a fact that seemed to contradict the physics of heat exchange. Consequently, Carey and his colleagues at the Woods Hole Oceanographic Institution set out to determine how this could be. As a consequence of their research program, we now know a great deal more about the temperature relations of large endothermic fishes.

The lateral swimming muscles of endothermic fish, such as tunas and mackerel sharks, are well supplied with blood vessels that function as countercurrent heat exchangers. These heat exchangers heat cool arterial blood as it carries oxygen to the lateral swimming muscles, and by the time this blood delivers its supply of oxygen and nutrients it has been heated to the same temperature as the active muscles. On the return trip the heat in this warm blood is used to heat the newly arriving blood and so, when blood exits the swimming muscles, it is again approximately the same temperature as the surrounding water. The countercurrent heat exchangers of tuna are efficient enough at conserving heat that these fish can elevate the temperature of their swimming muscles up to 14℃ above the temperature of the surrounding water. The anatomy of the countercurrent heat exchange in bluefin tuna muscle is presented in figure 4.23.

FIGURE 4.23 Countercurrent heat exchange in the lateral muscles of bluefin tuna. Carey and his colleagues implanted devices that would measure and transmit the temperature of the muscles of bluefin tuna and of the surrounding water. Their tracking boat could usually follow a released fish carrying a temperature-sensing implant for a few hours, which provided enough time to collect data that revealed a great deal about their temperature relations. As one of the monitored fish swam through water varying in temperature from 7°to 14℃, the temperature of its swimming muscles remained a constant 24℃. These results, shown in figure 4.24, demonstrate that a bluefin tuna can maintain a remarkably constant body temperature even in the face of substantial variation in water temperature.

FIGURE 4.24 Water temperature and body temperature of a bluefin tuna (data from

Carey 1973).

Now. let's move from the sea and the giant bluefin tuna, which can reach up to 1,000 kg, to land, where we find some of the smallest endotherms. Many terrestrial insects have evolved the capacity to heat their flight muscles. Warming Insect Flight Muscles

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. As we saw in chapter 1, bumblebees maintain the temperature of their thoraxes, which house the flight muscles, at 30°to 37℃ regardless of air temperature. Because they can warm their flight muscles, bumblebees can fly when environmental temperatures are as low as 0℃. 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℃. Despite these low temperatures, some of the larger moths captured had thoracic temperatures of 46℃, 9℃ 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 temperatams. It was clear. 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 alter- native 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℃. 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℃, the thoracic temperatures approached the lethal limit of 46℃. An interesting debate between two groups of researchers with competing hypotheses was decided by two decisive experiments, which are summarized by figure 4.25.