Temperature is a major determinant in biogeography, that is to say, it exerts a very profound influence on the distribution of animals over our planet. Temperature also sets limits on the activities of animals. Behavioral ecologists often discuss thermal activity ranges, the ranges of environmental temperatures over which animals can remain active. The range of environmental temperatures on the planet Earth is much greater than the temperature range that permits active life. Yet insects stand premier among land animals in their ability to inhabit the Earth's extreme temperature environments. Their ability to live, and carry out a full range of life activity, in environments ranging from hot deserts to high mountains to the high arctic depends, in large part, on various physiological responses to temperature. These responses vary from long-term seasonal synchronizations of life cycles to immediate behavioral and physiological adjustments. These short-term adjustments - behavioral and physiological - permit some insects to sustain a stable thoracic temperature while exposed to a rather broad range of ambient temperatures. The ability to maintain a stable body temperature while exposed to a range of varying environmental temperatures is called temperature regulation or thermoregulation. As with many areas of insect physiology, thermoregulation is a study of comparative physiology. Due to differences in body form and biology, the thermoregulatory mechanism in bumblebees, for example, is much different from a thermoregulatory mechanism that is quite adaptive in butterflies.

When we consider how an organism functions in nature, it becomes plain that the overall thermoregulatory strategy is nearly always a composite of both behavioral and physiological components. For example, bumblebees - which have quite impressive capabilities for physiological thermoregulation - fly at various heights from the ground in the arctic so as to remain in air that is about 8 to 10 oC. This behavioral aspect is a very important component of the overall thermoregulatory strategy of arctic bumblebees. We will operate in a somewhat artificial context in this section by limiting ourselves to mostly physiological mechanisms of thermoregulation. The limitation is a reflection of time constraints, and is not meant to take away from the importance of behavioral mechanisms of thermoregulation.

Let us begin with a consideration of the adaptive benefits that attend the ability to regulate body temperature. In general terms, insect flight is supported by a set of biochemical machinery that must be maintained within a relatively narrow temperature range for efficient operation. The ability to maintain the particular body temperature permits flight in a rather wide range of environmental temperatures. Maintaining a stable body temperature is not in itself sufficient information to conclude that an organism is competent to thermoregulate; thermoregulation implies an animal is able to maintain a stable body temperature while exposed to a more or less broad range of ambient temperatures. For example, honeybees forage at ambient temperatures ranging from 7 to 46 oC while maintaining a thoracic temperature of about 31 to 32 oC. Similarly, some butterflies fly at ambient temperatures as low as 7 oC, all the while maintaining thoracic temperatures near 37 to 38 oC. As a consequence of thermoregulation, butterflies can operate in such environments as cool mountain tops and the high arctic. Depending upon one's point of view, flight in itself is not important except perhaps as recreation. I expect you to regard the various areas of the biological significance of flight in insects. The point to be taken is that thermoregulation has broad biological importance in terms of broadening the thermal activity niche of insects.

Let us turn, now, to the physiology of thermoregulation during flight. We begin by noting that the temperature of an object at any instant in time is a balance of the rate of heat production and the rate of heat loss. Having juxtaposed temperature and heat in the same sentence, here are definitions of these terms: heat is a form of energy. By contrast, ttemperature is the integral of heat or a measure of heat content. In theory, the temperature of an object could be regulated by controlling either heat production or heat loss or both. However, during insect flight, the rate of heat production is necessarily high because of the intense and continuous muscular work demanded by this mode of locomotion. Due to mechanical and biochemical inefficiencies, as much as 80 to 90% of the energy expended during muscle contraction and wing movements appears as heat in the thorax rather than as power output for flight.

During the 1960's there was a great deal of contention over the mechanism of thermoregulation in some large insects, especially sphinx moths. This issue turned on the question of whether thoracic temperature was regulated by controlling heat loss or by modulating heat production. It is now clear that the rate of heat production depends upon the work performed in flight. Insects can not reduce the amount of work they perform in order to keep themselves aloft below a minimum dictated by aerodynamic constraints. Hence, insects can not reduce heat production for thermoregulatory purposes. In about 1970 it was first shown conclusively that heat loss was adjusted to stabilize thoracic temperature in the sphinx moth Manduca sexta. This work stimulated a tremendous interest in thermoregulation in insects. Since then, several insects have been studied, and all of them vary the rate of heat loss from the thorax to regulate thoracic temperature during flight. Let us now consider some of the mechanisms of regulating heat loss.



Sphinx moth, Manduca sexta


During flight at low ambient temperature, thoracic temperatures in this moth may be 20 oC higher than the temperature of the abdomen and 23 oC higher than the ambient temperature. But at high ambient temperatures, the abdomen can become almost as warm as the thorax and effectively operate as a thermal radiator. At higher temperatures, thoracic heat is transferred to the abdomen by movements of the hemolymph. During flight heat is produced by the flight muscles. The thorax is highly insulated by a thick coat of scales that appear in the form of a dense pile. Further, the thorax is thermally isolated from the abdomen by an insulating air sac. Recall that the insulating properties of air sacs is another adaptive role of these structures. At low temperature the heart and ventral diaphram beat at fairly low rates and relatively little of the thoracic heat is transferred to the abdomen by hemolymph flow. At the other extreme, at high thoracic temperatures the rates of heart beat and ventral diaphram action increase, and the hemolymph flows between thorax and abdomen much faster. A much increased rate of heat transfer between the thorax and abdomen follows. Heat is radiated from the virtually uninsulated abdomen to the environment. This last is shown by the rapid drop in temperature in the ventral section of the abdomen. The figure also shows an important anatomical feature of thermoregulation. The aorta loops between the left and right dorsal longitudinal muscles, thereby allowing substantial heat exchange between flight muscles and hemolymph.

How was this mechanism worked out? First we want to look at the business of measuring temperature. A fever thermometer is a little largish for this kind of research on insects. One technique was to build tiny thermistors. Thermisters are devices which are really just temperature sensitive transistors. Thermisters are quite small and they can be build into small probes. The probes are small enough to be implanted into various insect body segments. The thermistors are hooked up to an appropriate electrical bridge and actual temperatures are read from a calibration curve. An even better technique relies on thermocouples, which are made by coupling wires composed of different metals. A tiny flow of current trickles through the thermocouple junctions, and the flow changes as a function of temperature. Thermocouples can be small enough to implant several different couples into one insect without interferring with the insect's ability to fly. By implanting several different thermocouples, it is possible to monitor the movement of head within an insect body.

Now, let us consider some experiments with thermocoules. First, we can examine the influence of hemolymph flow on thoracic temperatures. If the heart is ligated at the first abdominal segment, thoracic temperature stabilization is abolished, and thoracic temperature zooms. We infer from this experiment that hemolymph flow is crucial for thermoregulation. Second, we can test the influence of thoracic scales on thermoregulation. If insulating scales are removed form the thorax, flight can be carried out at higher ambient temperatures, even with the heart tied off. Again, we infer that the thoracic scales are important elements of thermoregulation in large moths.

In addition to M. sexta, other sphinx moths regulate the thoracic temperature during flight, but the regulatory mechanisms have not been analyzed in detail. The dragonfly Anax appears to rely on a similar mechanism. When the dragonfly's dorsal heart is tied off, as in Manduca, heat transfer from the thorax is abolished. Also, some large beetles are thought to thermoregulate by a similar mechanism, but this remains to be shown in detail.




Bumblebees regulate thoracic temperature over a wide range of ambient temperatures during flight and they have a well-developed mechanism for circulating hemolymph between the thorax and abdomen. As in Manduca, hemolymph circulation is regulated so that heat loss from the abdomen to the environment is modified according to thoracic temperature.

In many Hymenoptera, including bumblebees the heart loops down through a narrow petiole such that warm hemolymph from the thorax must pass backwards through the petiole in close contact with cool hemolymph flowing forward from the abdomen. This anatomical arrangement creates a counter-current heat exchanger. Counter-current heat exchangers occur widely in vertebrate systems, such as in pelagic tuna or arctic foxes, where it is important to restrict the flow of heat from the core of the body. In bumblebees, heat from the thorax is transferred to the cool hemolymph coming from the abdomen. Thoracic heat is not transferred to the abdomen by direct flow of hemolymph. You can imagine that at very low ambient temperatures this is a surpurb adaptation form avoiding heat loss.

On the other hand, if heat can not be transferred out of the thorax, flight activity of bumblebees would be restricted to times and places of very low ambient temperatures. That is, the thermal activity niche of bumblebees would be restricted. The anatomy of bumblebees makes it impossible to separate the warm thoracic hemolymph from the cool abdominal hemolymph in space. It turns out that warm and cool hemolymph are separated in time. Heat is transferred from the thorax to the abdomen by pumping alternating pulses of warm hemolymph from thorax to abdomen, then cool hemolymph from abdomen to thorax. The overall scheme is fundamentally similar to the mechanism seen in sphinx moths: temperature regulation is achieved by controlling hemolymph circulation.

In warmer ambient temperatures, the bumblebee abdomen expands, drawing air through the spiracles into the abdominal air sacs. Simultaneously, the ventral diaphram is raised, creating suction in the abdomen. This allows a bolus of hemolymph from the thorax to enter the abdomen. Then the abdomen contracts, and abdominal air sacs deflate, thereby forcing air into the thorax. Just as this occurs, the ventral diaphram is lowered in the petiole and in this lowered position it simultaneously increases air passage into the thorax while reducing the passage of hemolymph out of the thorax. Meanwhile cool hemolymph from the abdomen enters the thorax without coming into contact with the warm hemolymph from the thorax.

What we imagine, then, is that the counter-current heat exchanger serves to keep heat in the thorax under cool conditions. Under warmer conditions, heat from the thorax is transferred to the abdomen by separating warm and cool hemolymph in time. This system turns out to be enormously adaptive. It allows flight activity in an impressively wide range of environmental temperatures. It is also used by queen bumblebees to incubate broods during the early days of their annual colony cycles. Brooding increases the rate of egg maturation, which translates into enhanced rates of colony development. This is particularly important for bumblebees in northern temperature zones, where relatively short colony seasons prevail.




A slight modification of this thermoregulatory mechanism occurs in honeybees. Due to several loops in the heart within the area of the petiole, honeybees have a continuously operating counter-current heat exchanger. This exchanger can not be circumvented by moving hemolymph in pulses. With this anatomical arrangement, the honeybee abdomen can not be used as a variable heat radiator. Instead, honeybees use an evaporative cooling mechanism that allows them to fly at unusually high ambient temperatures, up to 46 oC. During flights at high temperatures honeybees repeatedly regurgitate a droplet of fluid and suck it back in.

The essential experiments on this system were carried out on honeybees restrained at on a laboratory bench as room temperatures, about 24 oC. The honeybees were then heated with a microscope illuminator. When the insects gained heat, a fluid droplet appear on their faces. Within seconds, these insects underwent a 2 to 8 oC decrease in head and, just a bit later, thoracic temperature. This occurs rapidly because head and thoracic temperatures are strongly coupled due to passive conductance and to hemolymph flow from thorax to the head. Evaporative cooling may be of special adaptive significance in honeybees because they often concentrate dilute nectar solutions into honey. Evaporative cooling has also been reported in another sphingid moth, Pholus, which also repeatedly regurgitated and recovered a drop of fluid. Desert cicadas reduce their body temperatures by transporting water to their body surface though special water transport glands.

So far, this discussion has centered on maintaining stable thoracic temperatures during flight. We now turn to a consideration of initiating flight during low ambient temperatures. Larger insects are able to warm themselves prior to flight by activating the flight muscles with characteristic motor patterns. We consider a hawkmoth in three phases of warm-up. These are early warm-up, late warm-up and fight. In early warm-up the wing movements are small and the antagonistic muscles are excited at the same time. Later, as the thorax is warmer, the excursion of the wing movement is larger and the motor patterns are shifted such that the antagonistic muscles contract with less overlap. Finally, in flight the wing strokes are large and the antagonistic muscles are excited alternately. The small, rapid wing movements have been observed in several insects. I studied this in medium sized butterflies like the mourning cloak and monarch butterflies. This activity is correctly called shivering. There are, by the way, non-shivering mechanisms of generating heat in certain mammals that depend on biochemical adaptations. These have been thought to function in some insects as well, but the idea is not generally accepted.

Because the pre-flight warm-up only sets the stage for flight, we expect that minimum time and energy would be invested in warm-up. In this case it would be reasonable to keep as much heat as possible in the thorax to reduce cooling. In Manduca, Bombus, and the dragonfly Anax the abdominal temperatures remain within a few degrees of ambient temperature during warm-up. Hemolymph flow in each insect is regulated to avoid heat transfer.

Finally, we finish with a discussion of thermorgulatory strategies and terminologies. Large mammals, for example, sustain high and constant body temperatures through a relatively wide range of ambient temperatures, as you all have experienced personally. This is called homeothermy and such animals are called homeotherms. Still other animals generally conform their body temperatures to within a degree or two of the ambient temperature. This is called poikilothermy. Insects that regulate their thoracic temperatures to a high and stable level during flight do not fit into either category satisfactorily. These animals maintain high and stable temperatures part of the time in part of their bodies. They are correctly called heterotherms, referring to both features of thermoregulation.

Large insects are not the only heterotherms. In the tropics there are heterothermic hummingbirds and heterothermic moths. These animals are within a similar size range of 2 to 4 grams. They all feed on nectar while hovering in front of flowers. Heterothermy also occurs commonly in small bats and in several families of rodents.

What advantages might attend heterothermy, as compared to homeothermy? When aroused and active, heterotherms have the advantages of thermoregulating animals such as substantial physiological independence from environmental temperature. But when inactive, these animals share the frugal patterns of energy expenditure characteristic of poikilotherms. Large animals are probably too big to be heterotherms due to the effects of thermal inertia.

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