Thermoregulation in insect

Thermoregulation in Insect

Bemd Heinrich

University of Vermont

In insects, as in other animals, body temperature strongly affects the rate of energy expenditure, the rate at which food can be located and harvested, growth, the facility with which mates can be acquired and predators avoided, and sometimes also the susceptibility to disease organisms. Thermoregulation refers to the ability to regulate that body temperature which best serves survival and reproduction, and it encompasses numerous conflicting constraints and selective pressures. In insects, major considerations involve body mass and access to either external or internal heat. Thermoregulation operates through behavior, physiology, and morphology. For the most part, insects are too small to be able to appreciably elevate, or regulate, their body temperature by internal heat production, although some are large enough and that, coupled with their high flight metabolism, could easily cause them to overheat. In numerous insects, elaborate mechanisms of thermoregu­lation have evolved both for heating and for cooling the body that possibly rival those of the typically endothermic vertebrates.

ENDOTHERMY IN FLYING INSECTS

Insects arose on earth at least 350 mya in the Devonian Period of the Paleozoic Era. Little is known about the earliest forms, except that originally they must have been crawlers, not flyers, and their bodies assumed approximately the temperature of the immediate surroundings to which they adapted. This holds true even when the immediate surroundings are quite frigid. The adult form of a flightless midge (Diamesa sp.) walks on glacier ice even when its body temperature is chilled to — 16°C. It is so sensitive to heat that, when taken from its natural environment and held in one’s hand, it is killed by the warmth of one’s skin. However, there are insects that maintain quite specific and high body temperatures. Some species of sphinx moths, for example, have thick insulating fur and normally maintain a thoracic temperature near 46°C during flight over a wide range of ambient temperatures. To these moths, our own normal body temperature of 37°C is almost cool. An insect’s head and abdominal temperatures are for the most part unregulated.

In the same way that the motor heats up when a car burns fuel, heat is released as an inevitable by-product of cellular metabolism whenever muscle contracts. Close to 94% of the energy expended by muscles during contraction is degraded to heat, while approximately 6% appears as mechanical force on the wings. Insect flight is one of the most energetically demanding activities known, and thus most insects produce more heat per unit muscle mass when they fly than almost any organism on earth. Most insects exist under conditions somewhere in between the cold-blooded crawler and the hot- blooded flyer, but these extremes show us what is possible, and they thus offer us a remarkable window into thermal adaptation from an evolutionary perspective.

The ability of birds and mammals to regulate body tem­perature at one set point, specifically 37—4l°C, has long been considered proof of sophistication and phylogenetic advance­ment relative to animals whose body temperature varies with that of their environment. Deviation of body temperature from the set point of 37—4l°C is, in birds and mammals, often associated with illness and was once thought to be caused by a failure of the thermoregulatory system. We now know that both increases and decreases in body temperature can be and often are adaptive responses. Both responses are often sophis­ticated physiological mechanisms that involve more ther­moregulation rather than less, albeit the body is kept at a more appropriate temperature for specific conditions.

Small insects have much lower body temperatures in flight than large insects, not because they produce less heat—in fact, they may have higher rates of heat production than larger insects, but because they have much greater conductance because of their large relative surface area. In bees, for example, only the large species heat up in flight and generate an appre­ciable elevation of body temperature even though metabolic cost of flight per unit weight declines approximately 230% for a 10-fold increase in mass. A mosquito in flight maintains only a tiny (<1 a="" ambient="" amounts="" and="" between="" blow="" despite="" fly="" gradient="" heat="" i="" of="" prodigious="" production.="" temperature="" thoracic="">(Calliphora vicia)

may heat up 5°C, and a honey bee heats up its thorax about 15°C. Having a much larger thorax, and hence a smaller relative surface area, means that the internally generated heat during flight is not lost by convection at the same rate that it is produced until a much higher temperature gradient has been generated.

Large insects—those that inevitably generate a high body temperature during continuous flight—must be biochemically adapted to operate their flight muscles at the high temperatures experienced. Temperature is important for mechanical effi­ciency; at low muscle temperature there is partial overlap in contractions of the up- and downstroke muscles, the

dorsoventral and dorsal longitudinal muscles; the two sets of muscles then work against each other rather than working to move the wings.

Numerous other moths—such as most microlepidoptera and geometrids (inchworms) and some ctenuchids and arctiids—are small or weak flyers that do not heat up but fly at low air temperature. They fly at muscle temperatures much lower even than those at which the large-bodied, small-winged (and hot-blooded) sphinx moths generate zero power. Evolu­tion has acted strongly to tailor the flight motor’s capacity for maximum power output for much lower ranges of operating temperatures. For example, the geometrid Operophtera bruceata can gain sufficient power to fly at 0°C. (Nevertheless, its capac­ity to do so is only partially the result of muscle physiology.)

The basis for the evolution of differences between species arising from a common ancestor is variation among indivi­duals. Variation was present in the past, and for many traits, variation is maintained even now. For example, in Colias (sulphur) butterflies, the gene locus for phosphoglucose isomerase, one of the enzymes involved in energy metabolism in these butterflies, changes in allele frequency with season and habitat temperature. This suggests that natural selection is occurring even over very short (that is, seasonal) time spans. The different enzyme alleles have different thermal stabilities, and heterozygotes are thought to have an advantage in an envi­ronment of rapidly fluctuating temperatures inasmuch as the individuals heterozygotic for this locus fly over a range of tem­peratures broader than that of individuals of other genotypes.

When a seasonally changing temperature environment, which is the rule, can select for heterozygosity, then one might expect that an environment of constantly high or low temperature, which is the exception, should lead to the fixa­tion of an appropriate genotype. Hence, selection in terms of gene-frequency changes would not normally be present for our inspection in more constant environments, in which appropriate genotypes would already have been selected long ago to adapt to the average temperature. The specific thoracic temperature that is maintained by regulation is “chosen” by evolution probably because it is the temperature most readily regulated for maximum activity over a range of prevailing environmental conditions.

WARM-UP BY SHIVERING

During his classic studies of honey bee communication, Karl von Frisch noted that bees often interrupted flight for a few minutes when they were returning to the hive heavily laden with nectar. He presumed they stopped “to rest,” but we now know they were stopping to work: to raise their thoracic temperature. They most likely stopped flight because it was a cold day and they had cooled convectively. Bees are able to raise their thoracic temperature by shivering, which can work their flight muscles harder than flight itself does. Von Frisch could not have known any of this, because shivering and thermoregulation by individual insects was unknown in the 1960s, nor is shivering externally visible in bees even if one looks very closely.

Like the maintenance of an elevated body temperature by internal heat production in flight, physiological warm-up is found in all large, active flyers among the dragonflies (Odonata), moths and butterflies (Lepidoptera), katydids (Orthoptera), cicadas (Clypeorrhyncha or Homoptera), flies (Diptera), beetles (Coleoptera), and wasps and bees (Hymenoptera). That is, it is found from some of the earliest forms, the Odonata, to the most evolutionarily highly derived, the Diptera, Coleoptera, and Hymenoptera. It is not found in the small and therefore nonendothermic members of the same groups. Because no insects shiver except those that then also heat up from flight metabolism, it seems reasonable to conclude that the evolu­tion of shivering behaviors is related to the evolution of flight but is unrelated to the insect’s place on the phylogenic tree.

During preflight warm-up, there are synchronous contrac­tions of groups of muscles that normally contract alternately in flight. That is, the main wing-depressor muscles, the dorsal longitudinal muscles, are excited simultaneously—in other words, in synchrony—with the dorsoventral wing elevator muscles. The neural activation pattern of thoracic flight mus­cles needs to be and is already very labile for flight control, and to add shivering when flight behavior has already evolved is probably a very minor evolutionary step. Physiological warm­up in its most basic form is like the idling of an engine; the engine “evolved” to propel the car, not to warm it up. Once present, the heat-producing flight muscle system required only a slight modification of neuronal activation patterns and, in the more sophisticated models, also the addition of the bio­logical equivalent of a clutch—a mechanism to disengage the wings in the same way that an automotive clutch disengages the car’s wheels. Some insects, such as dragonflies and moths, do have visible external wing vibrations that were originally called “wing whirring,” these were once thought to pump air into the animal before the true function was elucidated.

The zenith of the shivering response of any hot-blooded animal (vertebrate as well as invertebrate) belongs to some bees. Honey bees and bumble bees have a physiological sophisti­cation either not existing or not yet observed in other insects, and they exploit shivering behavior to an unprecedented extent and in a variety of ways. Like flies and beetles, bees are “myogenic” flyers in which the wing-beat cycle runs in part on automatic; as the downstroke muscles contract they stretch the upstroke muscles. This stretching by itself causes the upstroke muscles to contract. The downstroke of the wing therefore automatically causes the upstroke muscles to contract and vice versa, in a repeating cycle that is sparked by neural commands that are at a much lower frequency than the wing beats and are no longer specific to a single wing beat. (This system permits some of the smallest insects, such as midges, to achieve the unprecedented coordination required for wing-stroke cycles of over 1000 beats per second.) But the stretching of opposing muscle groups that maintains the myogenic contraction cycle can occur only if the wings are actually beating—namely,

during flight. When the wings are not in use, as when they are folded back dorsally and the clutch-like wing hinge is engaged, then the muscle groups are in near tetanus. That is the reason for the bees’ shivering.

Very vigorous shivering in bees is physically dampened even more by yet another mechanism. One of the two sets of opposite- acting muscles is activated (and hence contracted) slightly more than the other. Because the opposing muscles act like weights forcing down each side of a seesaw, the added force on one set of muscles prevents the “seesaw” from working (and the wings from “vibrating” back and forth).

WARM-UP BY BASKING

Like warm-up by shivering, warm-up by basking occurs in all major orders of insects that have fast flyers large enough to heat up from their flight metabolism. In its simplest form, behavioral warm-up is merely heat-seeking. A basking insect usually takes specific postures that simultaneously maximize solar input and minimize convective heat loss. Heat input is maximized by exposing the maximum surface area to the sun, while convective heat loss is minimized by using body parts (such as the spread wings) as baffles to retard air movement around the body. Orienting the body parallel to the air stream (as a wingless insect might do) would reduce the effect of convective cool­ing, but orienting the body perpendicular to the sun’s rays to facilitate heating should take precedence, because no heat loss can be minimized until heat is first gained. Grasshoppers, beetles, and flies use these basking methods. For some dragon­flies and butterflies the wings are especially important during warm-up in their role of reducing convective cooling.

Behaviorally distinct types of basking have been described in butterflies, although some (tropical) butterflies do not bask at all. In one type, called “lateral basking,” the butterfly closes its wings dorsally and then tilts to present either the right or the left wing and body surface to the sun. The lower portions of the wings wrap around the body and touch it, and warming the lower wing portions in sunshine then causes heat to be conducted directly through them and into the body.

Many species of small-bodied butterflies, primarily pierids and some lycaenids (which commonly fly in breezy mountain meadows) bask by opening their wings partially in a V so that the body is directly available to the sun’s rays at the bottom of the V. The wings then serve as convection baffles to reduce cooling in the breezy environment. “Dorsal baskers” hug a solid substrate, such as the ground, and pull their wings down around them. They thereby expose the dorsal body surface to the sun while simultaneously capturing heat from the sun- heated substrate.

HEAT LOSS MECHANISMS

Insects near the size of a honey bee (approximately 200 mg) or larger may experience body temperatures during forced flight exercise that are potentially lethal to them. Alternately,

metabolic heating may inhibit continuous flight at relatively modest ambient thermal conditions (of air temperature and solar radiation), unless one or more of the following mecha­nisms for heat loss are activated.

Harnessing Convection

The rate of convective heat loss from a body is determined by the conductance of the body, i.e., its intrinsic rate of heat loss (which is a function of body size, shape, and insulation). Conductance, in turn, is a function of the wind speed (a hot body cools more quickly in wind than in still air— meteorologists call this the “wind-chill factor”). However, no convective heat loss is possible, regardless of conductance, if body and ambient temperature are equal, and at any one conductance and wind speed the amount of heat loss is directly proportional to the temperature difference between the body and the ambient surroundings.

Small insects that are endothermic in flight are sufficiently air-cooled such that they almost never reach the potentially dangerous high-temperature ceiling of near 45°C that is com­mon to most animal tissues at normal atmospheric pressures. These small insects thus have no need of a specialized cooling system: they lose sufficient heat passively. Theoretically, larger insects could cool themselves by increasing flight speed and thus increasing convective heat loss, but flying faster would generally increase metabolic heat production, which would cancel out the increased heat loss, unless the internally generated heat is redistributed.

Heat Radiators

A radiator is a device that increases the surface area of a body or object so that more heat can be transmitted to the surrounding environment by convection. In some radiators, a fluid with a high heat capacity (like water, blood, or other liquid) circulates by means of a pump and transfers heat from its source to the radiator site for the heat loss. That is how a car engine is cooled.

Radiators are utilized by many large insects from the very diverse orders Lepidoptera, Odonata, Dipera, and Hymenop­tera. The animals have a fluid-transfer cooling mechanism that dissipates heat through an abdominal radiator, while small members of the same groups that are not strong or continuous flyers lack the heat-transfer response. When we humans exercise in the heat, blood is pumped to the skin or extremities to facilitate heat loss, but this is done at the expense of pumping blood and oxygen to the muscles instead. Therefore, work capacity is compromised. Insects, on the other hand, do not need to compromise aerobic work capacity at higher air temperatures because of thermoregulation. In insects, the total separation of respiratory and heat-transfer functions makes it possible for them to continue working, even when the fluid flow is interrupted.

The “radiator tube” that conducts the hemolymph to the abdominal heat radiator in insects also serves as a pump,

which operates by peristaltic contractions along its entire length. Although sphinx moths in whom surgery has rendered this “heart” inoperative (by tying it shut) can still fly until reaching near-lethal thoracic temperatures, removal of their insulating layer of thoracic scales makes continuous flight again possible.

Evaporative Cooling

One of the extraordinary examples of an evaporative cooling mechanism specifically for thermoregulation is that found in the workers of honey bees, Apis mellijera, and yellowjackets, Vespula spp. These insects use the head as a radiator, but they do so with a difference. Nectar-gathering honey bees normally fly with flight-motor temperatures near 15°C above air tem­perature. They are capable of the astounding feat of flying even at ambient temperatures near 45°C while maintaining the thorax at the same or only slightly lower temperature. They do so by regurgitating nectar from the honeycrop, and while the nectar is held on the mouthparts and the head, water evaporates from it. Because of the physical contact between the head and the thorax, thermoregulation of one effectively results in thermoregulation of the other. Thus, the head is cooled by evaporation of water until there is a large tem­perature difference between the head and the metabolically heated thorax, at which point heat from the thorax follows the temperature gradient and is transmitted to the head. Head temperature is actively regulated, with thoracic temperature passively following, because artificial heating of the thorax alone does not result in the heat-dissipation response so long as head temperature remains low. However, artificial heating of the head (as with a narrow beam of light from a heat lamp) almost immediately results in nectar regurgitation and evapo­rative cooling, even while thoracic temperature is still (momen­tarily) low.

Some insects cool evaporatively from the back. In the hot Australian deserts, the larvae of the sawfly Perga dorsalis, in response to solar heat stress, first raise their abdomen to the sun to shade the body and to increase convective heat loss. In an emergency, when this response is insufficient, they also emit rectal fluid and spread it over their ventral surface to cool themselves evaporatively.

Diceroprocta apache of the Sonoran desert of the south­western United States employs a third evaporative cooling mechanism, this one analogous to sweating. These cicadas are plant-sap feeders, and despite living in a dry environment, they have access to a large fluid supply by inserting their sucking mouthparts into the xylem of deep-rooted shrubs, such as mesquite. They thus indirectly tap water from deep underground stores. Cicadas sing when ambient temperatures in the shade reach 40°C, and the repetitive contractions of their tymbal muscles result in internal heat production that adds to the already considerable external heat load.

Body temperature during this exercise in the heat is reduced to tolerable levels by evaporative cooling from fluid shed through large pores distributed over their dorsal body surfaces. The release of this fluid, and the consequent evaporative cooling, occurs only in response to very high body temperature. Most insects, especially those of desert environments, are instead highly resistant to water loss when alive, and upon death, there results an immediate increase in water loss as the spiracles are no longer actively maintained shut. Killing of the cicada, in contrast, immediately stops the sweating response, therefore showing that it is under metabolic control. The cooling response is mediated, ironically enough, by aspirin-like substances produced in their bodies in response to heat stress.

MORPHOLOGY AND THERMOREGULATION

Aside from physiology, various aspects of insects’ morphology come into play in their thermoregulating responses.

Insulation

Many hot-blooded insects that regulate their body tempera­ture have, like their endothermic vertebrate counterparts, bodies wholly or at least partially covered with insulation. One type of insulation is derived from air sacs. Insects already have air sacs used for breathing, and still air is, next to a vacuum, the best possible insulator. Many insects of various orders have air sacs between the thorax and the abdomen that greatly retard the leakage of heat into the abdomen. But large-bodied dragonflies have gone one step further: their air sacs surround the thoracic flight motor. The other two types of insulation are derived from exterior cuticular structures.

Lepidopterans are covered with a layer of thin overlapping scales, which are especially noticeable in coloring the wings. Rather than remaining flat and colorful for visual signaling as in butterflies, they have become long and thin to form a thick insulating body (thoracic) pile or fur coat in many moths. This coating of pile is so effective as insulation it more than halves the rate of heat loss, or doubles the temperature excess, hence permitting flight at much lower air temperatures. Endothermic insects with pile now fly in many northern areas and at times of the year at which they would otherwise be excluded. Conversely, insects from tropical environments have no or only sparse pile covering.

A covering of setae, small hair-like projections from the cuticle, is the third source of insect insulation. Setae have various functions and numerous independent evolutionary origins. Within the Hymenoptera, only the northernmost large bees, the bumble bees, have a heavily insulated flight motor. However, even honey bees have a layer of short insulating pile on the thorax, which aids them on cool mornings and at high elevations. Bees inhabiting the tropics and hot deserts do not have a covering of pile dense enough to provide appreciable insulation. But even tropical bees cannot get along totally without setae, because they use these projections to trap pollen from flowers. Some wasps, in contrast, live in the same northern areas that bumble bees do,

but they do not rely on pollen for protein. Instead, many are predators on fast-flying insects, and they are glabrous. Perhaps an advantage of fuel economy in flight, or perhaps the necessity for fast flight, has assumed more importance than drag-inducing insulation for thermoregulatory control.

Color

In a few instances, an insect’s color has a functional signifi­cance in thermal balance during basking. For example, lateral- basking sulphur butterflies (Colias spp., usually yellow or white) found in cool environments (such as mountaintops or high latitudes) or seasons (early spring) tend to have dark wing undersides. These darker individuals are able to heat up the thorax slightly faster than lighter congeners, which buys them additional flight time when basking is needed to prepare for flight.

Although color can have a slight thermal advantage, it is more often subservient to other needs, such as the need to evade predators. Not surprisingly, insects that inhabit open ground often match their background in color and thus are highly camouflaged.

Stilts and Parasols

A beetle walking on hot desert sand might experience tem­peratures that could kill it in a minute or less. Just a few millimeters above the ground, however, the hot, ground- hugging air layer is disrupted and mixed with cooler air from above. If we were shrunk to Lilliputian size and forced to live where a few millimeters’ difference in elevation could mean the difference between life and death, we would find some way to lift ourselves above the searing heat. Numerous ground- dwelling beetles living on hot sands do just that. Tiger beetles (Cicindelidae) begin to stand tall when sand temperatures exceed 40°C. Aside from extending their jointed legs to stand taller, some beetles, like Stenocara phalangium (Tenebrionidae) from the Namib Desert of southern Africa, have evolved very long stilt-like legs that allow them to avoid overheating by both avoiding the heat at ground level and losing some of the solar heat by convection through fast running.

Another option is to use one body part to shade another. For example, some beetles reduce their absorption of external heat from direct solar radiation by having an air space beneath the elytra that insulates the abdomen from direct solar radiation.

Countercurrent and Alternating-Current Heat Exchanges

At low air temperatures when the abdomen is cool, the flight motor could cool precipitously if the hemolymph carried heat away from the thorax to be dissipated from the abdomen. Two mechanisms, however, normally prevent this potential problem of thoracic cooling. The first is a temporary reduction or elimination of the circulation: to retard heat loss.

Another mechanism, one more subtle than cardiac arrest, helps some insects prevent heat leakage from thorax to abdomen. Proof of that is seen in honey bee workers and Cuculliinae winter moths, which never show appreciable increases in abdominal temperature, even as the flight motor stays hot. An examination of their circulatory anatomy explains the mystery: they harness countercurrent heat transfer.

A countercurrent implies two separate currents flowing next to each other but in opposite directions, as through the petiole between thorax and abdomen in insects. If the fluid in one current is of a higher temperature than that of the other, then heat (which is not confined by the vessel walls) will passively flow “downhill,” from high to low temperature, across these walls. Thus, if the hot blood leaving the thorax flows around the vessel in close proximity to cool blood entering it from the abdomen, as in most bees, then heat exchange is inevitable. At least some of the heat from the thorax will be recycled back into the thorax because the incoming blood is heated by the outgoing blood. In honey bees and winter moths, countercurrent heat exchange is greatly enhanced by prolonging the area for that potential heat exchange to occur, as the aorta in the petiole is lengthened and (in honey bees) convoluted into loops.

Bumble bees and northern vespine wasps have a very much different and seemingly less efficient countercurrent heat exchange circulatory anatomy than honey bees and winter moths (Fig. 1). This situation may seem counterintuitive because they live in cold climates, some species even inhabiting the High Arctic. They might thus be expected to have even better countercurrent heat exchangers than honey bees, which are of temperate and tropical origin. Instead of

Aorta

Insulation

■—Air sacs —

Ventral diaphragm

FIGURE 1 Anatomy of a bumble bee (Bombus) relevant to thermoregulation. The thorax is insulated with pile that reduces the rate of convective heat loss. The ventor of the abdomen is lightly insulated or uninsulated when the bee presses her abdomen onto brood to be heated. Hemolymph (blood) is pumped anteriorly by the heart, from the abdomen into the thorax. When dissipating heat from the working muscles in the thorax, the blood enters the aorta from the heart in pulses. Each pulse of cool blood from the abdominal heart into the thoracic aorta alternates with a pulse of warm blood entering the abdomen to the thermal window. In this way, countercurrent heat flow (into blood returning to the thorax) is minimized and heat flow (into the abdomen) is maximized. [Reproduced, by permission of Oxford University Press, from B. Heinrich, (1976),/. Exp. Biol. 64, 561-585.]

having more loops for countercurrent heat exchange, they have none! Nevertheless, their anatomy can also be understood in terms of thermal strategy, but as it relates to their social system.

Bumble bee and wasp queens start their colonies very early in the spring; each new queen attempts this task alone, as an individual. To this individual bee or wasp, time is of the essence, for she must complete the whole colony cycle within a single growing season. A queens first priority, then, is to rear a group of helpers. Temperatures when and where she builds her nest may be near 0°C, and if the brood were left at that temperature it might take years for them to develop to adults—provided they could withstand the freezing temperature. Even in the High Arctic, however, the queens of Bombus polaris can pro­duce a batch of workers in about 2 weeks, as can other bumble bees and Vespula wasps. Both bees and wasps accomplish these feats by incubating the brood from the egg to the pupal stage. The queens perch upon their brood clump—consisting of eggs, larvae, and/or pupae—and they press their abdomen upon the brood, much as a hen incubates her eggs with her belly. Only the abdomen provides a smooth surface for contact, but only the thorax produces heat by way of intense shivering by the flight muscles. No incubation, and hence social life, would be possible for these insects in a cold environment if, like honey bees, they were incapable of transferring heat from the source of its production into the abdomen that provides the smooth tight contact with the brood.

The bumble bees aorta is long enough to permit moderate heat exchange and hence retention of heat in the thorax, but it is short and straight enough so that a physiological mecha­nism can be activated that shunts the fluid and heat through, effectively eliminating countercurrent heat exchange.

Countercurrent heat exchangers in vertebrate animals can be bypassed by rerouting the blood into an alternate (generally external) channel. That is why our own veins seem to pop out when we are active in the heat. Such rerouting of the blood from internal to external channels is not possible, however, in insects with open circulatory systems lacking veins and capillaries. Instead, in bumble bees there is a physiological solution for heat loss in the presence of a countercurrent heat exchange anatomy that serves the same purpose as an alternate blood channel. In the bumble bee, this consists of an alternating-current flow of blood. To shunt heat past the heat exchanger and into the abdomen, the bee lifts a small valve that allows a pulse of warm blood to enter the abdomen, and in the fraction of a second after the warm blood enters the abdomen, she then squirts a bolus of cool blood into the thorax. And so it goes back and forth, hot and cold pulses of hemolymph passing alternately through the heat exchange area in the bee s waist. The essential point is that although the blood is not rerouted into a different channel, it is instead temporarily “chopped” into alternating pulses in the same channels. This is the opposite of countercurrent flow because instead of recovering heat from the thorax, the system acts to remove it, in this case into the abdomen.

The pumping of hemolymph by the heart and the ventral diaphragm is also aided by in—out pumping movements of the whole abdomen, which otherwise function only for moving gas in and out of the thorax; the in—out telescoping move­ments of the abdomen are synchronous with the heart beats and the ventral diaphragm beats, and they cause pressure changes that facilitate hemolymph flow in precise alternating currents.

THERMAL ARMS RACES Against Predators

On a summer day in the Sahara Desert in Algeria, as the sun rises and begins to heat the sands that have been cold at night, an abundance of insect life is forced to retreat to cool under­ground refuge. Those unfortunate ones caught out in the heat become disoriented and, moving frantically, they heat up even more, then they die. The sun keeps rising, and sand tempera­tures begin to exceed 46°C. The desert lizards, Accanthodactylus dumerili, continue to hunt the incapacitated prey and any ants they can find. But they now dash quickly across the sand, and when they stop and stand, they alternately lift their feet to prevent burning them. Meanwhile, long-legged silver ants, Cataglyphis bombycina, avoid the lizards by remaining in their burrows under the sand. However, they are poised to leave, waiting for the sand temperatures to heat up even more, until it reaches about 60°C, when the temperature of the air at ant height is about 46.5°C. Temperature “testers” among them lurk at the nest entrance. At the right moment, they signal the time to come out by releasing pheromones from their mandibular secretions. The rest of the colony then rushes out into the field to forage safely, until they too must retire back to their underground shelters—when they experience air tem­peratures of 53.6°C, which is just a fraction of a degree below their thermal death point.

In the southwestern deserts of the United States near Phoenix, Arizona, the desert or Apache cicada, D. apache, also engages in a thermal arms race against vertebrate predators. These cicadas are active at the hottest time of the year, and even then they wait until the high midday temperatures of 44°C (in the shade) near noon to be most active, when the cicada- killing wasps and birds are forced to retire from the heat.

In the deserts of southern California, the grasshopper Trimerotropis pallidipennis endures heat rather than regulating heat loss like the sweating cicada. By blending in with the background of the desert floor, it hides to escape bird and lizard predators. Normally grasshoppers that inhabit the ground stilt high above that substrate when it becomes heated to very high temperatures in sunshine. But to remain camouflaged it is imperative for T. pallidipennis to crouch down onto the searing hot ground. When that ground heats to near 60°C in sunshine, the duration of time that a grasshop­per can remain hidden is limited by how high a body tem­perature it can tolerate. T. pallidipennis has evolved to tolerate the extraordinary high body temperature of 50°C and can thus escape into the sanctuary of sunlight, where a predator such as a lizard or bird cannot hunt.

It is probably rare that insects escape predators by seeking out low temperatures. Possibly the best candidates are the Cuculli- inae, a subfamily of the generally endothermic Noctuidae or owlet moths. The Cuculliinae are a northern circumpolar group of moths, and in northern New England they may fly during any month of the winter when temperatures reach 0—10°C and when most of their bat and bird predators have left. During flight, cuculliinines have flight-motor temperatures near 30—35°C, as do other moths of their size and wing loading. Unlike all other moths, however, the cuculliinines can begin to shiver at the extraordinarily low muscle temperature of 0°C, and they continue shivering to warm up all the way to 35°C.

The giant hornets, Vespa mandarinia, attack honey bee colonies. During a typical giant hornet attack, a lone hornet forager first captures bees at the periphery of the bees’ nest. After several successful foraging trips to the beehive, the hornet deposits a marking pheromone at the hive entrance from the van der Vecht gland at the tip of the abdomen. This pheromone attracts other hornets from the home nest, and then the slaughter phase of the hornet attack begins: 30,000 bees can be killed in 3 h by a group of 30 to 40 hornets. Subsequently the hornets may occupy the hive itself, and then they carry off the bees’ larvae and pupae to feed to their own young.

The above happens when hornets attack colonies of the introduced European honey bee, A. melUfera, but the Japanese honey bee, A. cerana, has evolved an effective coun­terstrategy to the hornets’ mass invasion. With the latter, those unfortunate hornets that are recruited by the pheromone and then try to enter the hive are met and killed by heat as hundreds of bees envelop each wasp into a tight ball. The interior of these bee balls quickly rises to 47°C, killing the hornet but not the bees, whose upper lethal temperature is 48 to 50°C.

Against Competitors

Contest competition or fighting over food is rare in insects, but at least two species of African dung beetles, Scarabaeus laevistriatus and Kheper nigroaeneus, engage in combat over dung balls that they make to feed on and/or to serve as sexual attractants. An elevated thoracic temperature plays a crucial role in these contests on the ground. The more a beetle shivers to keep warm (with its flight muscles), the higher the tempera­ture of the leg muscles adjacent to the flight muscles in the thorax and the faster its legs can move and construct the dung into balls and roll it away. Endothermy thus aids in the scramble competition for food, and it reduces the duration of exposure to predators. Additionally, hot beetles have the edge in contest competitions over dung balls made by other beetles; in fights over dung balls, hot beetles almost invariably defeat cooler ones, often despite a large size disadvantage.

Mate Competition

For large insects, endothermic heat production is a requisite for flight, and it is during flight that other activities, including foraging, oviposition, and predator escape, as oppor­tunity and necessity dictate, may occur. Hence, to find a direct effect of body temperature on mating success specifically, one must examine a mating behavior that is not already tightly linked with some other temperature-dependent activity. Singing in some species is a good candidate. Singing is one activity that serves only for mate attraction, and in katydids and cidadas only males sing and the females remain silent. The vigor of this singing activity is associated with and dependent on thermoregulation. Katydids, Neoconocephalus robustus, warm up for their ear-shattering mating concerts by shivering, bringing flight-muscle temperatures above 30°C. Males of the Malaysian green bush cricket, Hexacentrus unicolor, sing from dusk until well into the night, and before they sing, they prepare themselves by shivering to achieve thoracic tempera­tures near 37°C. At thoracic temperatures of 37 to 38°C, the males are able to achieve the extraordinarily fast wing movements of up to about 400 vibrations per second.

The dragonfly Libellula pulchella demonstrates both the importance of body temperature for mating success and the trade-offs required for maximizing power output as an insect matures. The young, nonreproductive adults of this species are sit-and-wait predators that typically fly with relatively low thoracic temperature. Their flight-muscle performance does not peak at any one temperature; instead, performance is uni­formly spread over a wide range of low thoracic temperatures. In contrast, sexually mature males engage in nearly continuous flight in intense territorial contests. At such times, they generate a very high thoracic temperature, and they regulate that tho­racic temperature precisely and within only 2.5°C from their upper lethal temperature. Thus, muscle performance of the sexually mature males is narrowly specialized relative to that of young adults that do not engage in strenuous battle.

SOCIAL THERMOREGULATION

Many of the social insects regulate the temperature of their nests in coordinated behavioral and physiological responses involving the adult nest inhabitants. Nest temperature regula­tion functions primarily to maintain activity and to keep the otherwise thermally labile larvae at the proper temperature for rapid growth. Thermoregulation allows social insects to rapidly build up large nest populations and to inhabit environ­ments where they could not otherwise exist.

Nest Site

One of the first requirements for effective nest temperature regulation is the choice of an appropriate nest site. Typically, northern ants nest in the open, often under solar-heated rocks, or they make solar-heated mounds; many termites also nest to maximize exposure to solar radiation. Honey bees, that live in northern temperate climates require enclosed nest sites such as tree cavities, whereas a variety of other more tropical bees have open and exposed nests.

Nest Construction

Northern vespine wasps enclose their nests in multiple layers of paper that insulate the nest contents. Some termites and ants construct nests so located and constructed as to maximize solar heating in the morning and evening and to minimize overheating at noon. Nests may be constructed so that air circulation and heat transfer are enhanced for thermoregulation.

Behavior and Physiology

Ants regulate the temperature of their brood by carrying it to those parts of the nest with suitable temperatures. Both honey bees and vespine wasps regulate the temperature of the nest, especially near the brood. They fan to circulate air and carry off heat when nest overheating is imminent, and if temperatures continue to increase they carry in water and sprinkle it on the combs for evaporative cooling results. At low temperatures, such as during winter and in swarm clusters outside the hive, the bees crowd together tightly as air temperatures drop, thereby trapping heat inside. As air temperatures rise, the bees on the cluster start to disperse, the cluster loosens, and heat from the interior is released. In hives containing both honeycomb and comb with brood, the bees preferentially cluster around the brood. Brood temperature is maintained near 36°C in hives that may be subjected to air temperatures as low as —50°C and as high as 50°C, provided the bees have access to honey as an energy source for heat production in the cold and to water for evaporative cooling in the heat.