J. exp. Bio/. (1978), 74. *!-& 17With 17 figures

Printed in Great Britain

HEAT TRANSFER IN DRAGONFLIES: 'FLIERS' AND'PERCHERS'

BY BERND HEINRICH AND TIMOTHY M. CASEY

Department of Entomological Sciences, University of California, Berkeley, CA 94720ami Department of Environmental Physiology, Rutgers University,

New Brunswick, NJ 08903

{Received 19 July 1977)

SUMMARY

1. Both 'perchers' (Libellula saturata) and 'fliers' (Anax junius andAeshna multicolor) remained active in the field in sunshine at air tempera-tures from at least 24 °C to 36 °C.

2. The percher basked at low air temperatures and regulated exogenousheat input by postural adjustments. It markedly reduced flight activity athigh air temperatures but flew nearly continuously at intermediate tempera-tures.

3. In direct sunlight, the abdomen of L. saturata heated faster than thethorax, but this percher exhibited little or no capacity to transfer heatbetween abdomen and thorax.

4. In contrast, the fliers gave no evidence of behavioural thermoregula-tion, but both showed impressive capacities for heat transfer from thorax toabdomen.

5. When heated exogenously on the thorax the temperature of the entireabdomen of both fliers increased uniformly, but with endogenous heatproduction during pre-flight warm-up there was only a slight temperatureincrease near the anterior portion of the abdomen.

6. Removal of abdominal air sacs or immobilizing the abdomen with waxto prevent all abdominal pumping did not significantly alter the capacity totransfer heat from thorax to abdomen.

7. Ligation of the heart anywhere along the length of the abdomenabolished heat transfer. Given sufficient exogenous heat input, fliers that canregulate their thoracic temperature by transferring the excess heat to theabdomen died in about 2 min due to overheating when the heart wasoccluded. Under our experimental conditions the fliers appeared to thermo-regulate exclusively via a control of blood circulation.

INTRODUCTION

It has been assumed for a long time that dragonflies thermoregulate. Corbet (1962,pp. 125-133) discussed the possible role of various postures and behaviour patterns inthermoregulation and recognized two types of Odonata: those which, when active,remain continuously on the wing which he called 'fliers', and those which spend mostof the active period on a perch from which they make short flights, which he called

erchers'.

18 BERND HEINRICH AND TIMOTHY M. CASEY

May (1976) presented the first data on dragonfly body temperatures, giving direcUevidence that both perchers and fliers regulate their thoracic temperature. Heexamined primarily the role of postural adjustments of perchers to incoming solarradiation, but he also showed that the flier Anaxjunius could transfer heat from thoraxto abdomen. The fliers heat up the thorax during flight due to endogenous heatproduction, but the perchers heat up the abdomen while basking. We here examinephysiological mechanisms of heat exchange between thorax and abdomen in a largepercher and two large fliers.

MATERIALS AND METHODS

All of the dragonflies used in this study were captured by hand net along the creekat Del Puerto Canyon, Stanislaus County, near Patterson, California. Immediatelyafter capture the animals were confined in paper triangles, in 100% R.H. in a dark boxkept in the shade. They were used in the laboratory within 48 h.

We worked primarily with three species: Anax junius (Drury), Aeshna multicolorHagen (both Aeshnidae), and Libellula saturata Uhler (Libellulidae).

Field measurements included the timing of flight and perching durations. Durationsof activity of animals encountered by walking along the stream-bed of the Canyonwere timed to the nearest second with a stopwatch. Since individuals were notidentified it is probable that not all measurements were of different individuals. Bodytemperatures of tethered individuals were measured in ' still' (inside a cardboard boxwithin 20 cm high sides) and moving air (unbaffled and under field conditions whenanimals were active; air velocity was undetermined) with 36-gauge copper-constantanthermocouples using a portable Omega potentiometer. Animals were held in placebetween pins on a styrofoam pad, and the thermocouples were implanted about1-2 mm into the thorax and between the tergites of the abdomen. As examined anddiscussed previously (Heinrich & Pantle, 1975) the conduction of heat down the thinthermocouple wires has negligible effect on body temperature in relatively large insectssuch as dragonflies. Changes in body temperature were read at 10-30 s intervals afterthe animals had been exposed to direct solar radiation.

Temperature changes of thorax and abdomen during heating and cooling live anddead individuals in the laboratory were measured and recorded continuously on aHoneywell multichannel potentiometric recorder. As in the field, the animals wereheld in place with pins on a styrofoam pad. The tethered animals had one 36-gaugecopper-constantan thermocouple implanted in the thorax and 2-4 in the abdomen.Abdominal thermocouples were placed between overlapping tergites without piercingthe intersegmental membranes. They were glued in place with a mixture of moltenbeeswax-rosin. Heat was applied to either thorax or abdomen with a narrow beam oflight from an incandescent microscope lamp. Aluminium foil was placed betweenthorax and abdomen to minimize passive heating of the non-illuminated body part.Immediately following an experiment, the animal was killed by the injection of a dropof ethyl acetate and the experiment was repeated with all leads left in place. Unlessotherwise indicated, the heat lamp was in the same position to within 1 mm.

Passive rates of cooling were measured using recently killed animals and from thesemeasurements we calculated Newtonian cooling constants.

Frequency and relative amplitudes of the heart and the abdominal pumping

Heat transfer in dragonflies

Aeshna Libelluia

A

Aeshna

PleuronTergite

Sternite

Fig. i. Anatomy of the abdomen of Aeshna and Libelluia. Note difference in length and widthin the two species. Libelluia abdomen is shown while expanded and flattened (left) and whilecontracted (right). Cross section of abdomen of Aeshna schematically illustrates major internalbody parts surrounded by air sacs. Dashed lines show where wax was applied (see Methods) toprevent abdominal pumping.

movements were measured with paired electrodes connected to Model 2991 BiocomImpedance converters and recorded with a Beckman R411 dynograph recorder (fordetails see Heinrich, 1976).

In the dragonflies there is no telescoping of the abdomen during abdominalpumping; all abdominal pumping consists of lateral abdominal movements. In someexperiments, as indicated, we prevented abdominal pumping by glueing the ventrallateral edges of the tergites with beeswax-rosin (see Fig. 1). Where indicated, theheart was exposed by removing a dorsal section of an abdominal tergite and underlyingdorsal air sacs (Fig. 1). The heart, which we raised out of the abdomen with a bentinsect pin, was ligated with a human hair.

Blood volumes were measured by removing a portion of the dorsal abdominal

2 0 BERND HEINRICH AND TIMOTHY M. CASEY

40 r-

007.00 08.00 09.00 10.00 11.00 12.00 13.00 14.00 15.00 16.00

Time of day (h)

Fig. 2. Increase in air temperature in shade on a sunny day in late June at the Del Puerto studysite, and the abundance of Libdlula saturata (O) and Aeshnids ( x) {Anaxjumus and Aesknamulticolor) throughout the day.

tergites and withdrawing as much blood as possible with z fi\ capillary tubes. Thesevolumes thus represent only fluid that was not bound to the tissues. We made ourmeasurements only on living animals either immediately after capturing them, orwithin a day after capture while they had been maintained continuously at ioo% R.H.

RESULTS

Ecology and behaviour. In the area where we observed and captured dragonflies, airtemperatures were typically high and solar radiation was unimpeded by clouds. Inlate June, air temperatures in shade increased from 19-4 °C at 07.00 h to 36-8 °C at14.20 h (Fig. 2). Counts of animals seen along a 100 m section of the creek showedthat both groups of dragonflies peaked in abundance at intermediate temperaturesat 10.00-11.00 h and declined during the hottest part of the day. The Aeshnids wereabsent from the study area between 14.00 and 15.30 h, but we observed an occasionalL. saturata even during the hottest part of the day. At other times 2-6 animals couldusually be sighted at any one point in the study area.

The behaviour of the dragonflies changed markedly at different temperatures. TheAeshnids either flew 'continuously' (not seen to land) or they perched, invariably inthe shade. The perchers that remained visible at the study area throughout the daydisplayed a wide range of behaviour possibly related to thermoregulation. We did notobserve L. saturata until about an hour after the sun was on the study area. At the lowair temperatures (24-1-25-5 CC), in the early morning, they spent long durationsperching with the dorsum of the thorax and abdomen generally oriented at nearly rightangles to the incoming solar radiation (Fig. 3). At intermediate temperatures (27-5-31-0 °C), however, most animals encountered along the creek perched only for shor|

Heat transfer in dragonflies 2 1

400r

300

e% 20000c

100

4-24 26 28 30 32 34 36 38

Air temperature (°C)

Fig. 3. Perching durations of Libellula saturate at various air temperatures in the field.Indicated are means and ranges. Numbers represent sample size.

durations. At the highest air temperatures around mid-afternoon we recorded thelongest perching times. The abdomen of most of the afternoon perchers was generallyinclined vertical rather than being held nearly horizontal, and the animals tended toperch on the shady portion of plant stems. Until 11.00 h (29-5 °C) the abdomen of allperching animals was held 'horizontal'. The first instance of abdominal shieldingfrom the direct solar radiation was observed at 11.30 h (31 °C). By 12.30 h (33-5 °C)all perching of L. saturata was with negative orientation to sunlight.

Libellula saturata males appeared to be territorial. They generally used the sameperch, leaving it in an instant to chase another male that came near. The intrudingmale was generally chased only several metres at air temperatures of 36 °C or above.At air temperatures of 31 °C or less they obviously ' patrolled' an area such as a largepool. In one instance during an 8-5 min bout of continuous flight a male chased twomales out of the territory and copulated twice with a female. On another occasion amale patrolled a given area back and forth for 8 min without a single encounter withanother member of its own species.

High temperature reduced the incidence, durations, and intensity of chases inconspecifics. In the morning with air temperatures at 24-26 °C, mean flight duration

22 BERND HEINRICH AND TIMOTHY M. CASEY

1 2 3 4 5Time (min)

Fig. 4. The change in thoracic (•, + ) and abdominal temperatures ( x , •£) of dead Ubelhdasaturata tethered in full sunshine around mid-day in the field on a styrofoam pad (see Methods).Solid lines represent experiment inside a large cardboard box shielding the animal from thewind. Dashed lines represent heating while exposed to ambient wind conditions.

of L. saturata was 67 s (16-210), N = 15. Near mid-day at air temperatures of29-5-33 °C, these 'perchers' flew almost all the time. We observed flights in excess ofeight minutes, although flights as short as ios were also recorded during this period.At the highest air temperatures (36-37 °C), there was a precipitous decline in flightdurations of all individuals encountered in the study area. Mean flight time was 11(1-40)3, N = 19. Even when we chased animals from their perch they appeared tobe reluctant to fly; they returned to the same perch within several seconds. Flight andperching durations refer to animals that we did not disturb.

Even though the perching durations at low and high air temperatures were similar,the marked difference in flight duration resulted in much higher relative activity atlower air temperatures than at high. For example, at air temperatures < 26 °C theratio of flight to perching time was about o-6, while at air temperatures of 36 °C orabove it was about 0-07.

The direct solar radiation to which the dragonflies are exposed all day can have aprofound effect on their body temperature, especially in still air. Representativeheating curves of one of three animals examined are shown in Fig. 4. When we exposedrecently killed L. saturata to direct solar radiation in relatively still air at 13.00 h, boththorax and abdomen heated to approximately 50 °C within 4-5 min. Normally,convective cooling will reduce such rises in temperature. When we repeated the1

Heat transfer in dragonflies

45 -

U

Time (min)

Fig. 5. The change in thoracic (# ) and abdominal temperature ( x ) of a live and deadLibellula taturata tethered in full sunshine around mid-day in the field on a styrofoam pad

experiment with the same animals, this time exposing them to ambient wind condi-tions, the abdomen equilibrated at about 41 °C, and after 5 min the thorax was at only38 °C. We also examined heating of three live L. saturata in the field. Live animalsheated essentially like dead ones (Fig. 5).

Our field observations are consistent with the hypothesis (May, 1976) that Libel-lulids regulate their body temperature behaviourally. At air temperatures of 25 °C or

Heat transfer in dragonflies

40 -Thorax-<lead

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Fig. 6. Local heating of the thorax and abdomen of an individual Libellula saturate while aliveand immediately after death. The animal was not moved and thermocouple placement isidentical in all runs. In thoracic heating experiments the lamp was initially 3-5 cm above thethorax and moved to a distance of 5-5 cm when thoracic temperature was approximately 40 °C.In abdominal heating experiment the lamp was 8#s cm away from the abdomen to preventabdominal temperature from increasing too rapidly. Thermocouple placement: x , Ventralanterior abdomen behind the second abdominal segment; A, dorsal anterior abdomen, behindthe second abdominal segment; O, dorsal posterior abdomen, behind the eighth abdominalsegment; • , dorsal mesothorax. Air temperature is indicated by thin horizontal line.

less heat input is maximized through orientation to sunlight. At 26 °C to about 32 °Cthey are essentially continuous fliers; heat input and heat loss apparently balance outto produce an appropriate flight temperature. At air temperatures above 35 °C theendogenous heat production from flight is minimized by reducing flight time. Thecontinuous fliers showed no behavioural modifications with changes in air tempera-ture.

Another species of Libellulid dragonfly, Lepthemis collacata (Hagen), was visible inthe study area throughout the day. They were the first group to be active in themorning, and they remained active in bright sunshine. In contrast to Libellulasaturata, the Lepthemis collacata reduced the input of solar radiation at high airtemperature by raising the abdomen towards the sun (obelisk position) rather thanlowering it vertically behind the body. We observed no instances of the obeliskposition in the forenoon, but it was routinely observed at high (> 36 °C) air tempera-tures in the afternoon. Libellula saturata did not use the obelisk posture at any time.

Comparative anatomy. Despite dissimilar body masses, the perchers and the flierswe examined had similar thoracic masses (Table 1) but widely differing abdominal sizeand morphology (Fig. 1). Surprisingly, the perchers showed a thoracic mass which wasa higher percentage of total body mass than the fliers. The thorax of the fliers wasabout 44% t o t a l body mass (Table 1), while that of the perchers was 65%. Theabdominal mass of the percher was 16% body mass, in contrast with 31-35% in thefliers.

26 BERND HEINRICH AND TIMOTHY M. CASEY

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Fig. 7. Thoracic heating in live and dead Anax jumus. T, Ventral posterior abdomen behindthe eighth abdominal segment. Other symbols as in Fig. 6.

In the dragonflies, as in other insects, the heart is a thin tube extending the fulllength of the abdomen. However, unlike in most other insects, the heart lies beneathdorsal air sacs, rather than being attached close to the cuticle of the dorsum (Fig. 1).

Basic differences were observed in the circulatory systems of perchers and fliers.The circulatory system of the two Aeshnid species examined was considerably moresubstantial than that of the Libellulid. The maximum outside diameter of the heart inthe percher, L. saturata, was 0-12 mm, while that of the Aeshnids was o-25-O435 mm.Inside diameter of relaxed non-distended Aeshnid heart was about 0-25 mm. Thevolume of blood that we could readily extract by 2 fil capillary tubes from a wound inthe dorsum of the abdomen of recently captured animals was also markedly differentbetween perchers and fliers. Freshly captured L. saturata yielded on the average 11 -6 fil(N = 8) with a maximum of 24-6 fil (Table 1) while the similarly sized Aeshnamulticolor yielded approximately three times as much blood with a maximum of 49 fil.

Heat transfer. We wished to test whether or not the dragonflies can transfer heatfrom thorax to abdomen. The thorax is the site of heat production during flight, andthe abdomen is a potential site for the dissipation of excess heat to the environmentwhen the passive rate of heat loss from the thorax is not rapid enough to preventthoracic overheating to lethal (> 45 CC) temperatures. We supplied exogenous heat tothe thorax in stationary dragonflies and measured temperatures in the abdomen.

There was little heat transfer from thorax to abdomen or vice versa in the seven

24 r

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Heat transfer in dragonflies

i

U 16

e

12

4 -:-

\

f 4Thorax Abdomen Abdomen

(ventral, anterior) (dorsal, posterior)

Fig. 8. Data summary of heat transfer in Libellula saturata (stippled bars), Anax junius (solidbars) and Aethna multicolor (cross-hatched bars). Temperature excesses of thorax are due tothorax heating, but temperature increases of the abdomen are due to heat transfer. Tempera-ture excesses for ventral anterior and dorsal posterior abdomen represents difference betweenthe increases in live and dead animals. Horizontal line = mean, bars = range, and numbersindicate sample size.

individual Libellula saturata that we examined. When heated to 40-45 °C (about 200

above air temperature) either on the thorax or the abdomen, the temperature changeof the unheated body portion was nearly indistinguishable between live and killedanimals (Figs. 6, 8). During thoracic heating only the ventrum of the first abdominalsegment showed a slight temperature increase, averaging 1-30 °C, above dead controlanimals (Fig. 8). During abdominal heating, thoracic temperature increased on theaverage 176 °C (0-3-1 °C, N = 7) above that of dead controls.

The results of the heating experiments in Anax junius and Aeshna multicolorcontrasted sharply with those of L. saturata. The temperature of the abdomen in allten Aeshnids examined increased markedly when they were heated on the thorax. Theabdominal temperature increase was obviously not due to conduction since deadcontrol animals showed only a slight rise in abdominal temperature, and since thewhole abdomen increased in temperature relatively uniformly along its 4-5 cm length(Figs. 7, 8). However, the ventral anterior portion of the abdomen always warmed upto a higher temperature than the rest of the abdomen. In all Aeshnids examined (sixA. junius and four A. multicolor) the abdominal temperature increased 5-10 °C aboveair temperature when we heated the thorax to 40-45 °C (Fig. 8). These results clearlyshowed that the continuous ' fliers' examined have remarkable capacity to shunt heatfrom thorax to abdomen. On the other hand, Libellula saturata, a percher, has very

28 BERND HEINRICH AND TIMOTHY M. CASEY

34 x-

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30

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I8.I 24

22

20

182 3

Time (min)

Fig. 9. Thoracic (•) and abdominal ( x ) temperatures (ventral, anterior) during pre-flightwarm-up of Anax junius.

limited capacity to shunt heat from thorax to abdomen, or from abdomen tothorax.

Pre-flight warm-up. We implanted thermocouples in thorax and abdomen andobserved body temperature changes during pre-flight warm-up (shivering). In oneAnax junius (Fig. 9) and one Aeshna multicolor the rate of thoracic temperature increaseby endogenous heat production was similar to that obtained in our exogenouslyheated animals. As already observed by May (1976) the animals heated duringpre-flight warm-up apparently transferred little heat to the abdomen since abdominaltemperature remained low, significantly increasing only after the termination ofwarm-up. The five L. saturata we examined were either unwilling or unable to warmup by shivering in the laboratory. Through continued prodding and pinching of anindividual for several minutes, the maximum increase in thoracic temperature byendogenous heat production was just under 2 °C despite more or less continuous wingmovement.

Abdominal pumping. While at rest, dragonflies, like many other insects, ventilate thethoracic musculature by rhythmic contractions of the abdomen that drive air to andfrom the abdominal air sacs. This so-called abdominal pumping was conspicuous inall three species of dragonflies we examined, particularly during thoracic heating.Since abdominal pumping activity occurs during thoracic heating, it is correlated withheat transfer. We therefore examined in detail whether or not the pumping wasrelated to heat transfer mechanisms.

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Fig. io. Frequency, relative amplitude and relative pumping force of abdominal pumpingduring heating (•) and cooling (O) of the thorax in several Libdlula saturate. Relativeamplitude is derived by comparing the amplitude at any given thoracic temperature againstthe maximum amplitude recorded through an entire cycle of heating and cooling of thorax andabdomen. Pumping force represents the product of the frequency and relative amplitude.

In L. saturata the pumping frequency and the pumping amplitude increased withthoracic temperature during both thoracic heating and cooling (Fig. io), even thoughabdominal temperature remained relatively stable. During abdominal heating, on theother hand, the relative pumping force during abdominal pumping generally showed asharp decline with increasing abdominal temperature (Fig. n ) . Libellula saturataheated on the abdomen typically contracted the abdomen, changing its shape from flatto triangular (Fig. i). Because of this response the animals presented less surface areato the incoming radiation. As the abdomen contracted, the relative pumping move-ments of the abdomen became shallower and often declined to zero. However, untilpumping movements disappeared altogether, the pumping frequency increased (Fig.»)•

The Aeshnids, which transferred heat to the abdomen, had a qualitatively similarabdominal pumping response to thoracic and abdominal heating to that of theLibellulids, which showed little or no heat transfer.

We occluded the meso- and metathoracic spiracles in two Anax junius and the rateof heat transfer to the abdomen was greatly diminished. However, since the animalsalso ceased struggling and became limp it does not follow that the abdominal pumpwas involved in heat transfer; blocking the spiracles could have prevented removal ofcarbon dioxide that inactivates the heart (see Heinrich, 1976).

Heat transfer without abdominal pumping. In order to determine whether or not theAbdominal pumping is functional in heat transfer we selectively eliminated either the

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BERND HEINRICH AND TIMOTHY M. CASEY

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4 5 E (a) Intact(1st run)

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1 2 3

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Fig. i a. The change in anterior ventral abdominal temperature ( x ), posterior dorsal abdominaltemperature (O), and thoracic temperature ( • ) during (a) thoracic heating in live intactAeshna multicolor, (6) after the abdomen had been waxed to prevent abdominal pumping (seeFig. i) , and (c) immediately after death. The intact animal was run first and the abdomen wasthen waxed.

Heat transfer in dragonflies 31

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Fig. 13. The change in anterior ventral and posterior dorsal abdominal temperature (a) duringthoracic heating in intact Anaxjunius, (b) after the abdomen was waxed to prevent abdominalpumping, and (c) immediately after death. In this experiment the abdomen was waxed first.The wax was later removed and the experiment indicated at left was then performed. Symbolsas in Fig. 12. The sudden dip in thoracic temperature of the dead animal was due to a move-ment of the heat lamp.

abdominal pumping or the action of the heart. Abdominal pumping movements of theAeshnids were totally eliminated by waxing together the ventral portions of thetergites of each abdominal segment. In the animals examined (three Anaxjunius andtwo Aeshna multicolor) loss of pumping movements had little if any effect on heattransfer (Figs. 12, 13). Insects without the pumping movements increased abdominaltemperature during thoracic heating to similar levels as intact animals, although thetemperature of the abdomen rose less rapidly. In general, the dragonflies showed thegreatest rise in abdominal temperature during the first heating run. Thus if the insectwas measured first unoperated and then with waxed tergites, the second run tended toshow some decrease in heat transfer performance (see Fig. 12). However, the decreasewas not due to the experimental treatment, because if the animal was first run whilewaxed, and then run again with the wax removed, there was more heat transfer whenthe abdominal pump was blocked than when it was intact (Fig. 13). It is probable,therefore, that the animals' performance deteriorates from one run to the next, andthat abdominal pumping has only a minor or no effect on thoracic-abdominal heattransfer.

Heat transfer by blood circulation. We observed in live dissections of Aeshnids asfell as in Libellula that the heart and ventral diaphragm pulsations were generally, but

32 BERND HEINRICH AND TIMOTHY M. CASEY

Heart Thoracic heating

Abd. pumping

Heart Abdominal heating

Abd. pumping

10 sec

Fig. 14. Mechanical activities of the heart and concurrent abdominal pumping during thoracicheating and abdominal heating. During the portions of the runs indicated, thoracic tempera-ture increased from 29 to 39 °C, and abdominal temperature increased from 26 to 32 °C. Bothheating runs were performed in the same LibeUula taturata and the electrical leads remained inthe same location. Note amplitude increase of abdominal pumping and synchrony with heartpumping during thoracic heating. During abdominal heating the two were not synchronous.

not always, at the same frequency as the abdominal pumping movements. Theseobservations were, in part, verified by mechanical recordings (Fig. 14).

We examined the role of blood circulation in heat transfer by ligating the heart. Toligate the heart we cut away a portion of the dorsal abdominal tergites from one ormore segments and then pulled out the exposed air sacs, revealing the beating heartsurrounded by fat body. Two Anax and three Aeshna thus operated showed noimpairment of heat transfer to the abdomen during thoracic heating (compare Figs. 12and 15). We then partially lifted the heart with a bent insect pin and ligated it with ahuman hair. As a result the portion of the heart posterior to the ligation becamedistended and turgid (see Fig. 16), whereas the heart anterior to the ligation becamethin due to loss of fluid. Immediately after the heart was ligated the dragonflies wereheated on the thorax. Heat transfer was totally abolished. Although sham-operatedanimals transferred heat normally, those with a ligated heart showed no more heattransfer to the abdomen than dead animals, even though abdominal pumping move-ments were not diminished in frequency or amplitude (Fig. 15).

The transfer of heat to the abdomen was abolished both when we ligated the heartin the anterior or in the posterior of the abdomen. If thoracic temperature was allowedto stabilize we could immediately abolish the heat transfer by occluding the heart withforceps at the posterior tip of the abdomen (Fig. 17). Under these circumstancesthoracic temperature increased to 50 °C in 2 min while the temperatures in theabdomen declined. We infer from these observations that the blood is taken up in theheart near the posterior tip of the abdomen.

4 4 r (a) Live(sham operated)

Heat transfer in dragonflies

T (h) Live f (r) Dead(heart ligated)

33

6 0Time (min)

Fig. 15. The change in ventral anterior and dorsal posterior abdominal temperature (a) duringthoracic heating in a sham-operated A. junitu with damaged tracheal system (see Methods andFig. 16), (b) the same animal after the heart had been ligated with a strand of hair, and (e) thesame animal immediately after death. Symbols as in Fig. 12. The dip in thoracic temperatureof tho live animal (6) was due to movement of the heat lamp to prevent death.

In killed animals and those with a ligated heart, the temperature of the posteriorportion of the abdomen remained indistinguishable from that of the air, only theventrum of the first abdominal segment showed a slight rise in temperature. Since thistemperature rise occurred both in the dead and in the live (ligated) insects it must havebeen due to passive conduction (presumably due to the close proximity of the heatedthorax). On the other hand, the whole abdomen of the sham-operated animalsincreased in temperature. These results provide further evidence that the ventilationdid not account for significant heat transfer. Most or all observed heat transfer to theabdomen was accomplished by the circulatory system.

DISCUSSION

The primary objective of this study was to examine the roles and mechanisms ofpossible heat transfer between thorax and abdomen in ' percher' (Libellula saturata)pid 'flier' dragonflies (Anaxjunius and Aeshna multicolor). As 9hown by May (1976)

34 BERND HEINRICH AND TIMOTHY M. CASEY

A.junius can transfer heat from thorax to abdomen, but the mechanism had not beenelucidated.

Physiology of heat transfer. It is obvious that the Aeshnids have impressive capacitiesto transfer heat from thorax to abdomen (Figs. 7, 8, 12, 13, 17), whereas the Libellulidshowed little or no heat transfer either from thorax to abdomen or vice versa (Figs. 6,8). We can rule out the abdominal pumping as a primary mechanism of the observedheat transfer since both groups showed qualitatively similar responses to local heating,and since we experimentally blocked the pumping without significantly affecting theheat transfer (Figs. 12, 13). On the other hand, blocking the heart completely abolishesheat transfer (Figs. 15, 17). Therefore it is obvious that heat is transferred via theblood which must be pumped by the heart.

We do not know why abdominal pumping increases so significantly as the thoracictemperature increases unless it is associated with ventilation of the thoracic muscles.It appears, however, that the increased ventilation associated with thoracic heating isin excess of that which is needed to supply oxygen and remove carbon dioxide instationary animals unless they are struggling vigorously. Possibly the abdominalpumping movements coupled with the heart and ventral diaphragm action facilitatethe heat transfer, particularly at high temperatures when all three are rapid, asappears to be the case for bumblebees (Heinrich, 1976). Since the rise in abdominaltemperature was slightly more rapid in intact animals than in those without abdominalpumping (Figs. 12, 13), our data could suggest that the pumping may serve in afacilitating capacity for heat transfer, possibly by augmenting blood flow. However,our data are insufficient to come to conclusions on this aspect.

It is of interest that the Libellulid3 which lack the heat transfer capacity, or have itonly very weakly developed, are intermittent fliers, whereas the Aeshnids, the con-tinuous fliers that are unavoidably producing heat nearly continuously, have a well-developed mechanism to prevent over-heating of the thoracic muscles by shuntingheat to the long cylindrical abdomen. In our experiments the Aeshnids were thermo-regulating nearly exclusively by their control of blood circulation. But in free flightdragonflies frequently sail (Corbet, 1962) and until further measurements have beenmade we cannot rule out the possibility of some regulation of heat production throughvariation of durations and intensity of powered flight.

It is apparent that both Libellula saturata and Aeshna multicolor could generatesimilar thoracic temperature excess during given flight durations since both havesimilar thoracic masses and passive cooling rates (Table 1). The inability significantlyto regulate heat loss in L. saturata may thus be a factor limiting continuous flight,particularly at high air temperatures (Figs. 2 and 3). However, the small amount ofheat transfer from abdomen to thorax might be useful in basking in view of the morerapid heating rate of the abdomen in comparison to the thorax (Figs. 4, 5).

Heat transfer to the abdomen is minimal during pre-flight warm-up in fliers (May,1976). Heat retention in the thorax during endogenous warm-up (Fig. 9) is obviouslyof adaptive significance since the energetic cost of such warm-up would rise consider-ably if heat energy were to dissipate rapidly to the environment via the abdomen. Onthe other hand, animals which are 'inactive' (as were our tethered heated animals)would not have an energetic benefit in achieving and maintaining a high thoracictemperature.

Journal of Experimental Biology, Vol. 74 Fig. 16

Fig. 16. Photograph of dorsal anterior portion of Anax juniits abdomen restrained onstyrofoam pad with insect pins during heat transfer experiment. Dorsal portion of tergite offifth abdominal segment has been cut and folded posteriorly to expose the heart. The heart islifted out of the abdominal cavity with a No. 2 insect pin (o.d. = 040 mm). Note expansion ofthe heart to at least 05 mm posterior to the contact with the pin, and the threadlike appearanceof the heart where it contains little or no blood anterior to the occlusion.

B. HEINRICH AND T. M. CASEY (Facing p. 34)

Heat transfer in dragonflies 35

50 r

45

40

358.

J30

25

20

Heart pinched

10 12 14 16

Time (min)

Fig. 17. Stabilization of thoracic temperature by the transfer of heat to the abdomen duringthoracic heating of a sham-operated Anax jutrius with damaged tracheae. At the arrow theheart was pinched with forceps at the ninth abdominal segment (see Fig. 1). Symbols as inFig. 13.

Comparisons with other taxa. We have here demonstrated the physiological capacityto regulate body temperature by heat loss in two species of evolutionarily ' primitive'dragonflies of this already primitive insect group. The relatively ' advanced' dragonfly,Libellula saturata, lacked the capacity. It is of interest that more recently evolvedinsects such as bumblebees have fundamentally similar mechanisms of heat transfer(Heinrich, 1976). Even within the same sub-order (Anisoptera), different species ofsimilar size {Aeshna multicolor and L. saturata) do not necessarily rely on physiologicalheat transfer to regulate their thoracic temperature. Therefore the development of thiscapacity is apparently not related to taxonomic affinity. It has presumably evolved atseparate times in the same and different insect groups.

With the physiological capacity to dissipate heat at high air temperatures, insulationof the thorax is not necessarily a liability, but it may be an asset at low air temperaturesfor retaining heat. Dragonflies have little pile on the thorax, but the thoracic musclesare surrounded by air sacs that significantly retard convective cooling (Church,i960).

The capacity to control thoracic temperature by physiological heat dissipation hasalso been shown to be well developed in sphinx moths (Heinrich, 1970; Casey, 1976),insects which, like the Aeshnids, spend long periods in continuous flight over a widerange of ambient temperatures, and which are sufficiently large to elevate thoracictemperature by endogenous heat production. We speculate that all large insects willfcquire physiological heat transfer mechanisms in order to be continuously active in

36 BERND HEINRICH AND TIMOTHY M. CASEY

flight. Furthermore, they will probably not be limited by phylogenetic origin inmodification of the circulatory system to achieve this capacity.

Dragonflies have been on earth in recognizable form since the carboniferous.Present-day dragonflies, such as Anax junius weighing a gram or less, generate atemperature excess of up to 17 °C due to flight metabolism (May, 1976). Since eventhese relatively small fliers have modified their circulatory system for the dissipation ofheat generated in flight, we speculate further that if the large (wingspread up to about34 cm as opposed to 10 cm for A. juruus) Protodonate, Meganeura monyi, was anaccomplished flier, then it was probably one of the earliest endotherms withphysiological mechanism for the control of body temperature.

Supported by NSF grant GMS 74-18897. We thank Rosser Garrison for help inidentifying the animals and in locating suitable study sites.

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CASEY, T. M. (1976). Flight energetics in sphinx moths: heat production and heat loss in Hylet lineataduring free flight. J. exp. Biol. 64, 545-560.

CHURCH, N. S. (i960). Heat loss and body temperature of flying insects. II. Heat conduction within thebody and its loss by radiation and convection. J. exp. Biol. 37, 187-212.

CORBET, P. S. (1962). A Biology of Dragonflies. Chicago: Quadrangle Books.HEINRICH, B. (1970). Thoracic temperature stabilization by blood circulation in a free flying moth.

Science, N.Y. 168, 580-581.HEINRICH, B. (1976). Heat exchange in relation to blood flow between thorax and abdomen in bumble-

bees. J'. exp. Biol. 64, 561-585.HEINRICH, B. &PANTLE, C. (1975). Thermoregulation in small flies (Syrphus Bp.): Basking and shivering.

J. exp. Biol. 6a, 509-610.MAY, M. L. (1976). Thermoregulation and adaptation to temperature in dragonflies (Odonata:

Anisoptera). Ecol. Monogr. 46, 1-32.