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Flight energetics in sphinx moths: heat production and heat loss in Hyles lineata during free flight

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J. exp. Biol. (1976), 64, 545-560 With 10 figures

Printed in Great Britain

FLIGHT ENERGETICS IN SPHINX MOTHS:

HEAT PRODUCTION AND HEAT LOSS IN

HYLES LINE ATA DURING FREE FLIGHT

BY TIMOTHY M. CASEY

Department of Biology, University of California, Los Angeles, California 90024

(Received 20 August 1975)

SUMMARY

1. Mean thoracic temperature of free-flying H. Uneata in the field and in the laboratory increased from about 40 °C at Ta = 16 °C to 42-5 °C at

!Ta = 32 °C. At a given Ta, thoracic temperature was independent of body

weight and weakly correlated with wing loading.

2. The difference between abdominal temperature and air temperature increased from 2 °C at low T5 to 4-2 °C at high Ta. At a given Ta, the

difference between Ta^ and T* was positively correlated with thoracic

temperature.

3. Oxygen consumption per unit weight did not appear to vary with Ta

from 15 to 30 °C and was inversely proportional to body weight.

4. Thermal conductance of the abdomen (Cab) was greater than thermal

conductance of the thorax (Cth) in still air and at wind velocities up to

2-5 m/s. In moving air at speeds approximating flight, C^ was twice as high as in still air. Under the same conditions Cab was 3-4 times as high as in still air.

5. Thoracic and abdominal conductance are inversely proportional to their respective weights.

6. These data are consistent with the hypothesis that thoracic tempera-ture is controlled by regulation of heat loss. However, a heat budget derived from these data suggests that heat dissipation may not be sufficient to offset the decrease in passive cooling of the thorax at high ambient temperatures.

INTRODUCTION

Sphinx moths maintain elevated thoracic temperatures (Tlb) during flight that are

independent of ambient temperature (Heath & Adams, 1965; Heinrich, 1970). These temperatures result from high rates of heat production associated with flight (Zebe, 1954; Heinrich, 1971a; Heinrich & Casey, 1973) and lower rates of heat loss than most insects due to a dense layer of scales on the thorax (Church, i960; Heinrich, 1971 a). In the sphinx moth Manduca sexta, heat loss in flight appears to be regulated by varying rates of blood flow to the poorly insulated abdomen (Heinrich, 1970;

1971J).

In the white-lined sphinx moth, Hyles (formerly Celerio) Uneata, regulation of heat production has been inferred (Heath & Adams, 1965). Under confinement during periods of intermittent activity, H. Uneata can maintain a relatively constant thoracic temperature by alternate periods of cooling and pre-flight warm-up (Heath & Adams,

• Present address: Naval Arctic Research Laboratory, Barrow, Alaska, 99733.

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1967). Under natural conditions, however, H. lineata regularly engages in activity which requires sustained flight, making such a pattern of temperature regulation unfeasible; during foraging it flies continuously, and during migration this species flies for hours at a time (Grant, 1937).

H. lineata is particularly interesting in terms of temperature regulation because, unlike the situation in most sphinx moths, the body weight of different individuals in the field may vary fourfold. The present study examines the effects of body weight and air temperature on the flight energetics of H. lineata and the importance of the abdomen as a site of heat exchange.

MATERIALS AND METHODS

Moths were collected in the Mojave desert near Pearblossom, Los Angeles county, California, by attracting them to a u.v. lamp powered by a portable generator. Fifth-instar larvae were also collected in the same area of the desert and reared on various foodplants in the laboratory.

Body temperatures. Thoracic and abdominal temperatures were measured with a small thermistor (GC32SM2, Fenwal Instrument Co.) and read to the nearest 0*2 °C on a telethermometer. Thoracic temperature (Tib) was measured by thrusting the

probe into the centre of the thorax. Abdominal temperature was measured in the approximate centre of the abdomen by inserting the probe through the intersegmental membrane behind the third abdominal segment. The data were discarded if the temperatures were not obtained within 5 s of capture. Laboratory measurements of body temperatures were made within 2 days of capture. The moths were caused to fly in an 8-7 1 jar in a temperature-controlled room for at least three minutes before measurement of body temperatures. Moths were killed immediately after tempera-tures were taken by injecting a small amount of ethyl acetate into the thorax. In the laboratory they were weighed immediately. In the field, they were placed (in numbered paper triangles) in a box saturated with water vapour to prevent weight loss by evaporation, and weighed later on the night of capture.

Oxygen consumption. For measurements of oxygen consumptions during flight, moths were placed in an 8-7 1 jar immediately following pre-flight warm-up. The moths hovered readily, and if they began to settle the jar was shaken to cause them to con-tinue flight. Flight duration was timed with a stopwatch.

Before and after flight air samples were taken from the jar with a 60 ml syringe through a three-way stopcock cemented in the jar's lid. Chamber air was mixed by pumping the syringe several times before the sample was collected. Air currents set up by the moths' beating wings also helped to mix the air. Gas samples were injected through a tube of drierite and ascarite into a Beckman E-2 oxygen analyser. Oxygen consumption (s.t.p.) was calculated by the method of Depocas & Hart (1957). Data are presented only for continuous flights lasting longer than two minutes.

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[image:3.451.102.351.38.231.2]

Heat loss in a flying moth

547

Fig. I. Body dimensions in Hylet Imeata. (A) Mid-sagittal section showing insulation and general shape of the moth. (B) Measurements (arrows) made for calculation of surface area. Thoracic surface area calculated by assuming thorax is a cylinder of diameter dtb and length

/m. Abdominal surface area calculated by assuming the abdomen is a combination of a cylinder of diameter d^^ and length 1/2 Ub and a right cone of diameter d^t) at its base

and height 1/2 Ub.

45 °C in a constant-temperature cabinet and quickly transferred to the wind tunnel at 22 °C. Air flow in the tunnel was monitored with a hot-wire anemometer. Body temperatures and air temperature in the tunnel were continuously monitored with a multi-channel recorder.

Body dimensions. Body weights were measured to the nearest milligram. The moths were mounted with wings in flight position. When dry, the moths were photographed together with a millimetre scale, or the wings were traced. Photographs were enlarged to life size and wing areas were measured to the nearest 10 mm2 with a planimeter. Calipers accurate to o-1 mm were used to measure thoracic and abdominal dimensions and scale lengths. To calculate surface area, the thorax was assumed to be a cylinder and the abdomen to be a combination of a cylinder and a right cone (Fig. 1).

RESULTS

Thoracic temperature. During free flight, thoracic temperatures were relatively constant over a 16 °C range of air temperatures (Fig. 2). Thoracic temperatures of flying moths in the laboratory and in the field were about 40 °C except at the highest

la. (32 °C) where T^ increased slightly to 42-5 °C. The difference between Tth and

Ta varied from about 33 °C at an air temperature of 16 °C to 10-5 °C at an air

tem-perature of 32 °C. At air temtem-peratures of 35 °C or more the moths were reluctant to fly, and even when repeatedly stimulated did not fly for more than a minute.

At a given To, the thoracic temperatures of flying moths in the field were not correlated with body weight (r = 0-06, P > o-i; Fig. 3), but were weakly correlated with wing loading, the ratio of body weight to effective wing area (r = 0-53, P < 0-05; Fig. 4). These data are similar to those reported by Dorsett (1962) for sphinx moths from three species. However, the low value of the correlation coefficient indicates that much of the variability of Tth is not explained by wing loading.

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o

F

45

40

35

3

e

a. 25

20

15

6 5 16 7V

10 15 20 25 30 35 Air temperature (°Q

40 45

Fig. 2. The relation of thoracic temperature (7\i) and abdominal temperature ( 7 ^ ) to air temperature (T1,). Rectangles enclose ± 2 S.E., vertical lines indicate range, numbers indicate sample size. Black rectangles represent data collected in the laboratory, white rectangles represent data collected in the field.

Wing loading (N m"2) 5 7 9 1!

42

40

38

o

-o

o o

0

o

0

0

o o

o

o

1 o

0

1 1 t

42

3

1 40

E

38

0-3 1-2 36

H. lineata

50 70 90 110 Wing loading (mg cm"1)

Fig. 4

130 0-6 0-9

[image:4.451.104.319.43.288.2]

Body weight (g) Fig. 3

Fig. 3. The relation of thoracic temperature to body weight in free-flying moths in the field. Fig. 4. The relation of thoracic temperature to wing loading in free-flying moths in the field. Dashed line indicates the relation of thoracic temperature at take-off to wing loading in three species of sphinx moths, taken from Dorsett (1962).

Abdominal temperature. Unlike Ttb, abdominal temperatures of H. lineata

im-mediately following flight varied directly with air temperature. The difference between abdominal temperature and air temperature was small (maximum Tat —

Ta = 6-o °C) and the mean difference increased with increasing air temperature from

[image:4.451.41.409.349.532.2]
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Heat loss in a

549

30

29 G

3

e

8. I 28

| 27 o

1 26

00 O

1 1

36 38 40 42 44 Thoracic temperature (°C)

Fig. 5. The relation of abdominal temperature to thoracic temperature of moths during flight in the field. Line fitted by method of least squares. All data are collected on the same day at the same air temperature.

90

™ 70

o.

§ 8

50

30

0-3 0-7 1-1 1-5 Body weight (g)

1-9

Fig. 6. The relation of weight-specific oxygen consumption to body weight at several air temperatures during hovering flight of at least two minutes. Symbols: (D) T,= is °C, (O) T» = 23 °C, (A) r»="3O°C.Straight line = linearregression(r=o-73), curved line = power regression (r=»o-7s).

At a given T&, the abdominal temperature in flying moths was directly related to the thoracic temperature (r = 0-62, P < 0-05; Fig. 5). Heat production by the abdomen is negligible during warm-up and flight, and elevated abdominal tempera-tures result primarily because heat is transferred from the thorax to the abdomen. The correlation of Tab with Tih suggests that Tih is stabilized, at least in part, by

heat transfer to the abdomen (see Heinrich, 1970).

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Table i. Weight-specific oxygen consumption (ml 02 [g-h]-1) of free-flying

H. lineata at various air temperatures

T.(°C) X S.D. N

15 67-1 16-6 6 23 5 8 5 i6-a 11 3a 54-6 14-2 6

(g.h)"1 in a 1-5 g moth. The linear least-squares relation between log-transformed values of metabolism and body weight (g) is:

log M = — 0-53 log BW + 171 (ia) or M = 52-2 BW-°-<* (r = 075, P < o-oi). (1 b)

Although a hovering moth loses about twice as much heat passively from the thorax at ra of 15 °C than at Ta of 30 °C, the mean rates of oxygen consumption at the two

temperatures (Table 1) are not significantly different at the 5 % level (Student's t test). In H. lineata having similar body weights, rates of oxygen consumption are similar over a 15 °C range of air temperatures. These data suggest that metabolism during hovering flight in H. lineata, as in several other sphingids (Heinrich, 1971 a; Heinrich & Casey, 1973), is not correlated with air temperature. However, in view of the small sample size and large variability due to body weight, further data should be obtained.

Thoracic and abdominal cooling. In dead moths, thoracic and abdominal cooling was linear when plotted on semi-logarithmic co-ordinates (Fig. 7). The correlation coefficients (r) of linear regression equations for each individual cooling curve were 0*99. Such cooling is passive in accordance with Newton's law of cooling which states:

d

J±=k(T

b

-T

a

) (2)

where k is the Newtonian cooling constant, or rate of temperature change per ° C difference between body temperature (Tb) and the ambient temperature (Ta). The

cooling constant is 2-303 times the slope of the semi-log plot of Tb — Ta against time.

In still air, the abdomen cooled only slightly faster than the thorax, but as wind speed increased the difference between the cooling rates of the thorax and the abdomen also increased (Fig. 8). At a wind speed of 1 m/s or more, thoracic cooling was twice as rapid as in still air. Above 1 m/s thoracic cooling rates were similar. The cooling rates of the abdomen increased sharply at wind speeds of 0-5-1-0 m/s and only slightly between i-o and 2-5 m/s. At 2-5 m/s, abdominal cooling rates were about three times as rapid as in still air. Cooling rates of the thorax and abdomen are inversely proportional to body weight (Fig. 9).

To determine the relative rates of thoracic and abdominal heat loss in moths of different sizes, it is necessary to know how the weights of these tagmata vary with body weight. Since heat transfer is calculated on the basis of surface area, the relations of calculated thoracic and abdominal surface area to body weight are included (Table

2)

-Insulation. Scale lengths differ on different parts of the body. From Table 3 several

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Heat loss in a flying moth

55*

< i3

10

8 6 4

-a

- i i i i

0 1 2 Time (min)

0 1 2 Time (miri)

15 10 8 6 4 3

i i i i

0 1 2 Time (min)

[image:7.451.128.291.69.314.2]

0 1 2 Time (min)

Fig. 7. Semi-log plots of cooling curves for thorax ( ) and abdomen ( ) of a 0-95 g moth in (a) still air, and (6) wind of 2-5 m/s, and of 0-39 g moth in (c) still air and (d) wind of 3'5 m/sec.

0-9

0-8

I) °'

7

"e 0-6

E 0-4

00

I

0-3

0-2

Abdomen

Thorax

0-5 10 1-5 Wind velocity (m/s)

20 2-5

Fig. 8. The relation of thoracic and abdominal cooling rates to wind velocity. Mean values are connected, vertical lines indicate ± 2 8.E. Minimum n = n .

different parts of the thorax or abdomen the length of scales is not the same. In general, the scales on any particular part of the body are longer on larger moths.

[image:7.451.93.363.363.549.2]
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552

10

0-8

6 0-6 o

r d 1 V 0-4

0-2 j I

0-3 06 08

Body weight (g)

[image:8.451.108.313.50.284.2]

10

Fig. 9. Linear regressions of log-transformed thoracic and abdominal cooling rates to body weight at a wind velocity of 0-5 m/s.

Table 2. Allometric equations relating weights and surface areas of the thorax

and abdomen to total body weight

Where Y=aXl>; a is the Y intercept and b is the slope of the linear regression of

log-transformed data. All regressions are significant (i><o-oi).)

a b N r

Thorax Weight Surface area Abdomen

Weight

Surface area

0295 4-78

0-576 7 0 8

0 6 6

1 09

i-33 0-84

8

23

8

23

0 8 4 0 8 7

o-8i

0 8 1

Table 3. Length of scales on various parts of the body in moths of

different body weights, measured to the nearest o-1 mm

Body weight (g)

Dorsal thorax Ventral thorax Dorsal abdomen Ventral abdomen Lateral abdomen

0-30 3-o

I ' 2

0-4 °5

o-8

0-65 3-4

1 8

°'4S

o-6

i ' 3

I'lO

S-5

3 ' i

o-6

i - o

2'O

and convection. As such, it is affected by the characteristics of the animal, such as insulation, and also by the properties of the environment, such as radiative tempera-ture (TT) and the wind velocity. Physiologists have utilized the equation:

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Heat loss in a flying moth

553

45 r

1 o o 1 J= 1 60 (ca l tanc e o 3 T3 C 8 40 35 30 25 20 15 10 o -• -• -• i o 0 1 0 \

o

\

oS

o

o 1

o

">$ -o - i 6

- 5

o

4 : - 3 3 •o

§

01 03 Weight (g) 0-5

- 2 8

- 1-5

0-8

[image:9.451.94.363.62.281.2]

Fig. i o . Linear regressions of log-transformed values of weight-specific thoracic and abdominal conductance to thoracic weight and abdominal weight respectively at wind velocity of 0-5 m/s. Equations for the lines are presented in Table 5.

Table 4. Weight-specific thermal conductance (cal[g.h. °C]~y) of thorax (Ct)l) and

abdomen at various wmd speeds. Cal(g.h. °C)-X equals 0-1186 W(N. "C)"1

Wind speed S.D. Thorax N o-o 0-5 i-o i'5 2-0 2-5 o-o 0-5 i-o I S 2-0 3-5 11-64 1609 19-05 2I-IO 21-53 22-76 12-75 22-40 27-95 3I-OS 31-76 36-22 2-22 4-74 4-56 6 6 2 5-2* 4-38 Abdomen 3-6i 9-33 8-18 8 0 6

12-28 1287 16 14 1 2 13 13 i t 17 15 1 1 1 1 13 1 1

to describe the rate of heat loss (dHjdt) in animals, where C = thermal conductance and is obtained by multiplying the Newtonian coohng constant by the specific heat of animal tissue (for discussion of the relation of thermal conductance to whole animals see Bartholomew & Tucker, 1963; Tucker, 1965; Lasiewski, Weathers & Bernstein, 1967; Herried & Kessel, 1967; Bakken & Gates, 1974). This equation, predicting linearity of heat exchange, is somewhat simplified because the components of heat transfer do not always vary in a similar manner.

On logarithmic co-ordinates, weight-specific conductance of the thorax (Cth) and

[image:9.451.52.399.327.520.2]
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[image:10.451.56.403.118.221.2]

Table 5. AUometric equations relating toeight-specific thoracic and abdominal

con-ductance to thoracic and abdominal weight respectively at various wind speeds

(Symbols as in Table 3. All regressions are significant at least at the 0-05 level. Minimum N= n . )

Wind speed (m/s) o-o i-o 2-O a 4 3 4 3 6 9 4'5 7-4 b — 0-69 - 0 - 9 7 - 0 7 8 - 1 0 6 - 0 7 1

r

0 8 3 0 8 4 0-85 O75 o-73 a 7-9 11-a 15-1 n - a 14-1

6 -°-45

— 0-67 - o - S 7 - o - 4 3 — 0-69

r 0 7 2

0 7 7 o-86

0-76 0-87 6-8 - 0 8 3 083 186 -o-6o 083

Table 6. Data used in calculating heat exchange in moths of various body

weights flying at different ambient temperatures

(Thoracic and abdominal temperatures are mean values at various T» (Pig. 2). Oxygen consump-tion for moths of various weights calculated from equaconsump-tion (i) and converted to calories by assuming fat utilization (Beenakkers, 1969). Thoracic and abdominal weights calculated from equations in Table 3. Conductance of thorax and abdomen at wind speed of 0-5 m/s calculated from equations in Table 5. Values for heat production represent o-8 times the total energy expenditure.)

Body weight (g)

Heat production (cal/min) Thoracic weight (g) Abdominal weight (g) Cth(cal[g.h.°C]->)

Cr t(cal[g.h.°C]-i)

0-5 2-28

0186 0-229 2 1 9

33-a

i - o

3-14 0-296 0576 13-6

1 6 7

I -S

3-57 0-386 0-988

1 0 3

11 -2

(Fig. 10). Abdominal conductance is greater than thoracic conductance in still air and at all wind speeds tested (Table 4). The slope of Ctb is greater than the slope of

Cab as a function of weight, both in still and moving air (Table 5).

DISCUSSION

Energy balance in flight. Under steady-state conditions the heat lost by a flying moth must equal the heat produced if Ttb is to remain constant. Energy exchange

takes place from a variety of avenues in flying moths. Only about 20 % of the meta-bolic energy is converted to power. A portion of this 20 % (aerodynamic power) is transferred to the air and represents the rate of energy expenditure necessary to keep the animal aloft. The remaining portion (inertial power) is necessary to accelerate and decelerate the wings and is eventually lost as heat through the wings (see Weis-Fogh, 1972).

About 80 % of the energy expended is immediately degraded to heat which must be lost from the respiratory passages or from the surface of the body. An attempt will be made to quantify heat loss through various avenues to evaluate their importance for thermoregulation during flight. Pertinent data used in the calculations are given in Table 6.

[image:10.451.184.383.318.395.2]
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Heat loss in a flying moth 555

by Weis-Fogh (1964). In locusts there is apparently little abdominal heat loss (see Church, i960) so that the net heat loss is calculated only from thoracic temperature (Weis-Fogh, 1964; his equation 1). In sphinx moths, however, Tab is sufficiently

above Ta to make the abdomen an important site of heat loss. Consequently, net

heat loss should be subdivided into thoracic and abdominal components for analysis of heat loss in hovering sphinx moths, such that:

M « Pt h + Pa b + Pw + Pia+i), (4)

where M is the total metabolic rate, Pt h represents thoracic heat loss, Pa b represents

abdominal heat loss, Pw represents respiratory heat loss and P(a+o represents the

fraction of the metabolic rate which is converted to aerodynamic and inertial power. Assuming that Pla+<> is a constant 20% of M, and substituting equation (3) for

thoracic and abdominal heat loss, the total heat loss is:

3£- *= C

th

(T

ih

-T

a

) + C

ab

(r

ab

-T

a

) + P

W)

(

5

)

where Cth and Cab represent thoracic and abdominal conductance respectively.

Conductance values for the thorax and abdomen obtained from the cooling curves should be applicable to moths flying in the laboratory because (1) substrate conduction is negligible in the wind tunnel and does not exist in hovering moths, (2) radiative temperature of the environment (TT) is equal to the air temperature (in flying moths,

TT = temperature of the glass jar; in dead moths, Tx = temperature of plexiglass

wind tunnel), (3) cooling rates at wind speeds approximating those in flight were obtained (see Bakken & Gates, 1974). However, convective heat exchange in flying moths is very complex (see, for example, Chance, 1975) and is only crudely approxi-mated by a dead moth in a wind tunnel.

Respiratory heat loss. Heat may be lost in respiratory passages by evaporation and convection. Although a detailed analysis of respiration during flight in sphinx moths is lacking, a knowledge of oxygen consumption and the temperature of the thorax under various conditions may be used to estimate the rates of heat loss by evaporation from the respiratory passages during flight (Weis-Fogh, 1967; Heinrich, 19746). Relative humidity of 0% will be assumed so that calculated values will represent maximum rates of water and heat loss. The high rates of oxygen consumption asso-ciated with hovering flight (Fig. 6) necessitate substantial ventilation of the primary tracheae. The efficiency of oxygen extraction during flight in insects, birds and bats is about 4-7% (Weis-Fogh, 1967; Tucker, 1968; Thomas & Suthers, 1972). If H. lineata extracts oxygen from the incurrent air with an efficiency of 5 %, ventilation rates will vary from about 1460 ml (g.h)"1 in a 0-5 g moth to 760 ml (g-h)"1 in a

1-5 g moth.

The amount of water evaporated depends in part on the thoracic temperature during flight. At higher Tth, the saturation deficit is greater and more water is

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Table 7. A partial heat budget in hovering sphinx moths

((A) Heat loss by evaporation from respiratory passages at temperature and pressure of the working thorax in o % relative humidity. (B) Heat loss from the surface of the thorax. (C) Heat loss from the surface of the abdomen. Numbers in parentheses represent the percentage of the total heat production. Cal/min = 0-0697 W.)

A. Evaporative heat loss (cal/min)

Body weight (g) o-s i-o

Body weight (g) o-S

i-o

Body weight (g) o-5

i-o

' S

16 0-38 (17) o-5S (17) °S9 (17)

16 1 56 (68) i-54 (49) 1 52 (42)

16 024 (10) 0-32 (10) 024 (10)

23 0-40 (18) °-SS (18) 063 (18)

B. Thoracic heat loss (cal/min)

23 1-09 (47) 1-°7 (34) 1 03 (28)

C. Abdominal heat loss (cal/min)

23 044 (19) 0-56 (18) 064 (18)

3 2 0-47 (21) 064 (21) 073 (21)

3 2 o-7S (33) O74 (23) 073 (20)

32 o-S3 (23) 0-67 (22) 077 (22)

temperatures (Table ya). Since oxygen uptake does not appear to vary as a function of Ta, it is unlikely that heat loss is controlled by regulation of respiratory water loss from the thorax. If 02 consumption were lower at high Ta, less water would be lost

by evaporation. Abdominal ventilation of sphingids is slight and probably of little importance for regulation of heat loss during flight (Heinrich, 19746). Cuticular water loss is also too low to contribute significantly to the heat budget (Church, i960; Casey, unpublished observations).

In addition to heat loss by evaporation, heat is lost by respiration because the air is warmed while it is in the thorax. The specific heat of air is low, however, and respiratory heat loss by convection represents only a few per cent of the total heat production in flight and therefore may be neglected.

Thoracic heat loss. Even when a moth hovers in still air, there is a considerable air flow around its body because a mass of air equal to body weight must be accelerated downward through the wing to balance the weight. The rate of air flow (induced velocity) at the level of the beating wings, using body dimensions of H. lineata (Casey, 1976) and Pennycuick's (1968) equation (3), is about 0-7-0-8 m/s. To calculate heat loss, conductance at 0-5 m/s (Table 5) is used. Thoracic and abdominal con-ductance will be underestimated by about 5 and 10% respectively at this slightly lower wind speed.

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Heat loss in a flying moth 557

of 32 °C. At any given T&, smaller moths lose a greater fraction of their heat production

from the surface of the thorax than large moths. However, over the range of T&

employed in this study, more heat is produced than can be lost passively from the thorax.

Abdominal heat loss. The flight muscles are responsible for about 99% of the metabolism during flight in insects (Weis-Fogh, 1964) and it is unlikely that the abdomen produces sufficient heat to raise TBb above Ta. Abdominal temperature is

usually above Ta during flight, however (Fig. 2; Bartholomew & Heinrich, 1973),

because heat is transferred from the thorax to the abdomen via blood circulation (Heinrich, 1970; 1971 b). Although the moths cannot change their insulation, variation of heat loss can occur because added heat input to the abdomen causes local changes in the AT, particularly in the ventral abdomen. Temperatures measured in the centre of the abdomen should represent an average abdominal temperature because the temperature in the ventral portion is higher than that in the dorsal portion (see Heinrich, 1971 b). If the system is in steady state, with Tab stabilized and the rate of

heat input constant, abdominal heat loss may be estimated using equation (3). Calculated abdominal heat loss increases from about 10% of the total heat pro-duction at Ta = 16 to about 21 % at T& = 32 °C for moths of various sizes (Table

7 c). The increase in heat loss by the abdomen at high T», is not sufficient to offset the decrease in thoracic heat loss, and unless heat loss is regulated at some other point Ttb would continue to rise.

It should be emphasized that these data for abdominal heat loss rest on several assumptions. For example, the abdomen is not losing heat equally at all points due to variable Tab (Heinrich, 1971 b) and differences in insulation (Table 3). In addition,

heat loss may be greater than calculated values because the heat is delivered near the surface of the abdomen. It is likely that the major resistance to heat flow is provided by the scales and the muscles and cuticle which compose the body wall, but heat is not flowing from the centre of the abdomen outward to its surface, as occurs in the thorax (see Church, i960).

Regulation of heat loss. Thermoregulation in hovering sphinx moths must involve regulation of heat loss because metabolism apparently is not varied as a function of

Ta. In those species where regulation of heat loss is not involved, such as locusts

(Weis-Fogh, 1956) and Monarch butterflies (Kammer, 1970), a constant rate of heat production results in a constanttemperaturedifference(rth — T J over a wide range of Ta.

The rate of heat loss by the abdomen at any given Ta is limited by its conductance.

If all heat not lost by the thorax and by respiration (Table 8 a) is dissipated from the abdomen, by rearrangement of equation (3), it is possible to calculate the effective temperature difference of the whole abdomen. These temperatures (Table 8 b) ait much higher than Tab of moths in flight at various Ta (Fig. 2). At high Ta the moths

need an average abdominal temperature similar to Tth in order to dissipate the heat.

During flight at T* = 32 °C, Tab is about 7 °C lower than Ttb. Although heat loss

is facilitated at high Ta by blood flow to the abdomen, particularly when Tih is high

(Figs. 2, 3), these calculations suggest that Cab and Tab are too low in H. Uneata

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[image:14.451.66.389.151.315.2]

Table 8. Abdominal heat exchange if the abdomen is the only site of regulation

of heat loss

((A) Extra thoracic heat loss (Total heat loss minus thoracic heat loss minus respiratory heat loss) which must occur to maintain Ttt, at temperatures shown in Fig. a. Numbers in parentheses represent percentage of total heat production. (B) Average Tc,-Tt necessary to dissipate all excess heat from the abdomen.)

A. Extra-thoracic heat loss (cal/min)

Body weight (g)

o-s i-o i'5

B. (7»b— Tx

Body weight (g) o-S

i-o

16 o-34 (is) I 06 (34) 1-46 (41)

) necessary to dissipate

16 27 6-6 79

2 3 0-79 (35) 1-50 (48) 1-92 (54)

excess heat from the abdomen (°(

23 6-2 93 10-4

3 2 1-04 (46) 1-69 (54) 2-10 (59)

3 2 8 2 io-s 114

occur in the head, wings or legs. The wings would make excellent thermal windows because they have a high surface-to-volume ratio and are poorly insulated. In addi-tion, pulsating organs, which facilitate blood flow in the wings, are particularly well developed in sphinx moths (Brocher, 1919). Small size and poor insulation reduce the risk of overheating in most insects, but in sphinx moths high rates of heat pro-duction and a well-insulated thorax make overheating during flight possible even at moderate air temperatures. Heat loss by variable blood flow to the wings represents a potentially important avenue of heat exchange which should be examined in endothermic insects during flight.

Data from the present study and that of Heinrich (1971a) suggest that heat dissi-pation rather than heat conservation is important for sphinx moths during flight at ecologically relevant ambient temperatures. These data do not support a previously proposed model for heat exchange of endothermic insects during flight (McCrea & Heath, 1971; Heath et al. 1971). That model predicts that at Ta& below 30 °C, heat

loss from the thorax is so great that heat production must be increased by varying flight performance. However, calculated metabolic rates based on flight mechanics (McCrea & Heath, 1971) are several times lower than measured values (for discussion see Heinrich, 1974a; Casey, 1976). Sphinx moths fly at TaS as low as 7°C (Bartholomew & Heinrich, 1973). If the model were correct, the moths would be unable to fly at such low TaS due to excessive heat loss. Moreover, there are no data to show that insects vary their flight performance for thermoregulation. In bumblebees (Heinrich, 1975) and in several species of sphinx moths (Casey, 1976) the metabolic rate during hovering is related to wing loading, regardless of the air temperature.

Sphinx moths are capable of flight only when they maintain Ttb within a relatively

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Heat loss in a flying moth 559

'than the surface of the thorax. Since most sphinx moths are nocturnal, they probably do not see temperatures as high as 32 °C in nature. The heat production of moths during forward flight should be much lower than during hovering, and since moths probably do not hover continuously in nature, heat stress during foraging flights is probably not so extreme as to incapacitate them.

The lowest Ta at which flight is possible may well be determined by the ability

to elevate thoracic temperature by pre-flight warm-up. Heat production during warm-up is proportional to thoracic temperature (Heinrich & Bartholomew, 1971; Bartholomew & Casey, 1973). If Ta is too low, moths produce insufficient heat to

elevate Tth even when warm-up is continuous for up to thirty minutes (Heinrich,

1971a).

The energy budget in this paper assumes that oxygen consumption during flight accounts for all the energy mobilized. There is in vitro evidence to suggest that flight metabolism is aerobic (Sacktor, 1970), and indirect evidence to suggest that oxygen availability is not limiting during flight in locusts (Weis-Fogh, 1967). However, in the locust Schistocerca gregaria (Krogh & Weis-Fogh, 1951) and in the sphinx moth Metopsilus porcellus (Zebe, 1954) there is a significantly elevated post-flight meta-bolism, lasting over an hour. The significance of this phenomenon has not been resolved, and further in vivo data are desirable.

This paper forms part of a Ph.D. dissertation submitted to the University of California, Los Angeles. Support for this study was provided by National Science Foundation grant GB32947 to G. A. Bartholomew. I thank Dr Bartholomew for his guidance and support throughout my graduate career and particularly for his editorial comments and criticisms. Thanks are due to Dr F. Engelmann, Dr E. B. Edney, Dr B. Heinrich and Mr P. Withers for helpful comments and stimulating discussions, and to Dr K. A. Nagy and Dr F. N. White for reading the manuscript. My wife Kathy helped in all phases of this study.

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Figure

Fig. I. Body dimensions in Hylet Imeata.and height 1/2general shape of the moth. (B) Measurements (arrows) made for calculation of surface area.cylinder of diameter/m
Fig. 3. The relation of thoracic temperature to body weight in free-flying moths in the field.Fig
Fig. 8. The relation of thoracic and abdominal cooling rates to wind velocity. Mean valuesare connected, vertical lines indicate ± 2 8.E
Fig. 9. Linear regressions of log-transformed thoracic and abdominal cooling ratesto body weight at a wind velocity of 0-5 m/s.
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