Analysis of the Effect of Temperature on Insects in Flight Author(s): L. R. Taylor Reviewed work(s): Source: Journal of Animal Ecology, Vol.

32, No. 1 (Feb., 1963), pp. 99-117 Published by: British Ecological Society Stable URL: http://www.jstor.org/stable/2520 . Accessed: 21/12/2011 23:25
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99

ANALYSIS OF THE EFFECT OF TEMPERATURE ON INSECTS IN FLIGHT

BY L. R. TAYLOR Department of Entomology, RothamstedExperimental Station, Harpenden,Herts. Many attempts have been made to relate the numbers of insects in flight to some function of air temperature both outside and in the laboratory. The subject is complicated in nature because temperature affects both the level of population and the amount of activity of those insects able to fly. Natural populations are usually sampled by traps and current methods of analysis often attempt, first, to distinguish between population changes and behaviour changes and then to relate behaviour, or the amount of activity, to temperature by regression analysis of catches. The method has been applied with outstanding success by Williams (1940, 1961) to large taxonomic groups; its use is based on the hypothesis that activity increases gradually with increase in temperature up to an optimum; above this, further temperatureincrease causes a fall in activity. Linear regressions are fitted over short temperature ranges and the regression coefficients are positive up to the optimum and negative above it. The whole response curve has recently been demonstrated by Williams & Osman (1960) using trap catches from Egypt where monthly mean temperatures ranged widely enough to show the rise to the optimum, 18-29? C, and the decline above it, 29-34? C. In laboratory cages the number of flights made per minute by individuals of a single species frequently gives a similar response curve, one that rises gradually with temperature to an optimum and then falls gradually to zero, so that some laboratory results appear to be complementary to the regression analysis used by Williams. But flight in cages, being restricted, is not typical of free flight in the open and the number of flights per minute is very much affected by these experimental limitations. Also the increase in numbers flying in the open as temperature increases, shown by trap catches of large taxonomic groups, is caused by the increasing number of species in flight as well as by the number of individuals of each species. Suppose that each individual insect can fly only between two fairly clearly defined temperatures,a lower threshold and an upper threshold, and that all insects of the same species in the same local situation have similar thresholds, i.e. that temperaturethresholds are species specific. Then between these two thresholds, the proportion of insects in flight may well be independent of temperature. Hence regression methods may not be appropriate for the analysis of the temperature responses of single insect species. I have therefore analysed the numbers in flight in the open of five very different species of insect in relation to air temperature, to investigate both the effect of temperature on flight and methods suitable for its evaluation, in terms of this hypothesis. However, activity and population changes are chronological processes and trap catches are rarely instantaneous. I have therefore re-examined what a trap catch representsbefore attempting analysis and, after analysis, the results are considered in the light of laboratory observations.

100

Temperatureand insectflight

THE THEORY OF TRAP CATCHES The meaning of a trap catch The density of insects in the air is always changing and few insect species fly throughout both day and night. The numbers in flight of a day-flying insect during 24 h are shown in Fig. 1 by plotting numbers per unit volume of air, aerial density (p), against time (t). Insects fly during a time period (Tf), from t2 to t5, which varies from day to day. Trapping for a period of 1 h (Ti), from t3 to t4, gives a catch equal to the cross-hatched area (C1). Trapping for a period of a single day (T24), tl to t6, gives a catch equal to the whole shaded area (C24). However, C24is actually collected in period Tf, which is less than T24because no insects fly between ti and t2 and between t5 and t6, i.e. at night. For a night-flying insect the situation is reversed; there is no catch for several hours in daylight.
320 ---T 4 --

280280

__

_-

-- -- ---

- - - - - - 1- -- -

- - - - - - -

240-

U200L 0 0 160

L
T

~10

ti

t2

t~~3 4
OO.OOhours 06.00 AERIAL 12.00 DENSITY x 18.00 TIME (pxt)

t5

t G 00.OC

FIG. 1. The variation in numbers of an insect flying from hour to hour. The shaded area equals total daily catch; the cross-hatchedarea equals a single hour's catch. T24 is a 24 h trappingperiod; Tf is the flight period; T1is a 1 h trappingperiod.AphisfabaeScop., 4 July 1949,

Thus a 24 h catch, being the area under the curve for density in relation to time, may be written:
t5 C24
t2

dt(1)

where p is instantaneous aerial density, t is time, the trapping period is T24, and flight period is Tf, not T24.Tf is not necessarily constant from day to day. Williams (1940) made a significant step toward considering what, in a biological sense, constitutes a trap catch with the proposition that Catch is proportional to Population x Activity: C24 = kiPA, (2)

L. R.

TAYLOR

101

where Population, P, is the total available population and Activity, A, is the proportion in flight; ki is a constant. However the product of Population, P, and Activity, A, is more specifically the instantaneous aerial density, p, i.e. p -PA, and, therefore expression (1) becomes:
t5

(3)

C24-{PA
t2

dt.

(4)

Expression (2) is equivalent to expression (4) only if it can be assumed that (t5-t2) iS the same from day to day and that P and A are independent of t during the period T24. This is true enough for a first approximation with such heterogeneous material as a whole insect order in which Tf is wide and imprecise because of overlapping flight times. For single species, however, the concept of 'catch' is not susceptible to close analysis without further definition in time; the limits for summation are important. This distinction is not just academic. If a trap is emptied every hour, the definition of the catch in time is accurate enough. However, if the trap is emptied daily, clearly the length of time during the day that the insects were active, is at least as important in determining the total catch as the aerial density during that time. In fact, if aerial density remains fairly constant, catch is the simple product of mean aerial density (D = p) and the flying time (Tf), i.e. the effect of environmental factors as independent variates on the dependent variate, the catch, may be determined as much by the length of time they operate as by the intensity with which they operate. Because many environmental factors fluctuate daily within wide limits, and hence act for only a part of each day, this cannot be neglected in analysis. Anaylsis of activity in thresholdterms Williams (1940) also pointed out that total activity is the product of the (activity due to temperature)x (activity due to light) x (activity due to wind-speed), etc. According to the threshold hypothesis, activity for, say, temperature may take either of two values. Below the threshold flight is inhibited and activity is 0; above the threshold activity is not inhibited and activity is 1. The same is true for light, wind-speed, etc., if thresholds exist for these factors. Total activity A, therefore, is the product of Osand is and is itself 0 or 1. This obviously is true for a single insect. However, the threshold is not exactly the same for different individuals nor for different occasions and appears as a frequency distribution in a population. The chance of A being 1 on any particular occasion will increase as temperature increases through the threshold region and a probability distribution will appear, with repeated samples from a population in the field, corresponding to the threshold distribution for individuals within the population. The separation of''population'and 'activity' Williams was concerned with large heterogeneous populations of which he could reasonably assume that population changed slowly relative to T24 and therefore that successive day-to-day changes in catch, being more rapid, were promoted largely by activity. But Johnson's (1952) intensive analysis of flight in Aphisfabae clearly showed that population can sometimes change as rapidly as activity and the time differentiation used by Williams is not then valid. Use of a time differentiation to distinguish between activity and population changes

102

Temperatureand insectflight

assumes a regression response over a temperature range nearly as wide as normal temperature fluctuations. If the response is a threshold, any fluctuation in aerial density once the temperature is clear of the thresholds must be considered as fluctuation due to chance or to population. Such fluctuations can be largely eliminated by classifying the catches as 0 or 1. Hourly catches would then be 0 until the temperature rises up to the lower threshold, 1 whilst the temperature remains above the threshold, and 0 again when the temperature falls below the threshold. If the temperaturerises above the upper threshold during the day, there should be a period without a catch during that time. If the population remains constant, or if population fluctuations are eliminated by classifying catches, the relevant measure of the effect of temperature on activity is the length of the period duringwhich flight occurs, estimated by the number of sampling periods with a catch. This should be directly proportional to the time that temperature stayed between the lower and upper thresholds, i.e. measured flying period should give a linear regression through the origin when plotted against expected flying period. This assumes that the trap is sensitive enough to catch an insect whenever the population is active. If it is not, the chance element in the sample will be great and the threshold Table 1. The amountof daily variationinflying time explainedby thresholdanalysis
%

s2 explained

N Vespula germanica T.D.C. x E.F.P. Aphisfabae T.D.C. xE.F.P. M.F.P. x E.F.P. Rhagonycha fulva T.D.C. xE.F.P. M.F.P. x E.F.P. y x 27 24 24 14 14
= =

x 5.52* 24-96 24-96 22-25 22 25

y 3-11 923 24-97 12-29 7-71

r 0-629 0-153 0-843 0-467 0 552

P <0 001 >01 <0 001 <0 1 < 005

b 0-881 14-2 0 875 0-643 0 337

by b 40 2 71 22 30

T.D.C. (total daily catch) or M.F.P. (measuredflight period). E.F.P. (expectedflight period): * in hours; remainderin half hours.

distributions will be blurred by what amounts to lack of resolving power of the trap. A similar lack of sensitivity occurs when the trapping period is long relative to the rate of temperaturechange. Daily catches can be used only in relation to the daily maximum or minimum temperature for the lower or upper thresholds respectively. Hourly catches are liable to less error in this way. When only one insect is caught the mean hourly temperature may be more useful than the maximum or minimum because of the low probability of a single insect being caught at any one instant and the very short time that the maximum or minimum temperature lasts; with larger catches however, maximum and minimum temperatures should be used as for daily catches. TRAPS AND CATCHES All investigations were done on natural populations in their normal habitats. The insects were caught by various kinds of suction traps so that aerial density was measured directly. Experiment I An 18 in. (46 cm) suction trap (Johnson & Taylor 1955) was used at 41 ft (I 4 m) over a seedling oat crop for the month of May 1960. The trap was emptied at 15.00 hours daily

L. R. TAYLOR

103

giving a 24 h catch. Air temperature was measured continuously 200 yd (180 m) away, at 4 ft (IP2 m), in a Stevenson screen. Experiments 2 and 3 A 9 in. (23 cm) suction trap (Taylor 1951) was used at crop level in a mature crop of field beans in a walled garden for the month of July 1952; a segregating mechanism in the trap gave half-hourly catches. Temperaturewas measured at 1 ft (30 cm) and 4 ft (120 cm) in the bean crop by shielded mercury-in-steeldistance thermograph (Johnson, Taylor & Haine 1957). Experiments 4 and 5 Four 12 in. (30 cm) suction traps (Johnson & Taylor 1955) hung from a tower, one each at 9 ft (2-7 m) and 21 ft (6-4 m) and two at 56 ft (17 m), over a large expanse of poor pasture, during the autumn of 1953, 1954 and 1955 (Taylor & Carter 1961). Hourly catches were obtained and the catch from all four traps summed. Temperature was recorded by thermograph at 5 ft (1-5 m) in a Stevenson screen 200 yd (180 m) away. The catch The following insects were used for analysis: from Experiment 1, queen wasps of the species Vespulagermanica (Fabr.); from Experiment 2, the black bean aphid Aphisfabae Scop., alate alienicolae; from Experiment 3, the cantharid soldier beetle Rhagonycha fulva (Scop.); from Experiment 4, the noctuid moth Agrochola lychnidis(Schiff.); from Experiment 5, the noctuid Amphipyratragopoginis(Linn.); these names are after Kloet & Hincks (1945). ANALYSIS Exa'ple 1. Vespula germanica (Fabr.) Flight behaviour could best be studied in a population with a constant number of individuals, but artificial populations must be caged and this prevents free flight. In contrast, natural insect populations have free flight but rarely have constant numbers. However, in spring 1960 the queens of V. germanica were unusually common after hibernation and this seemed likely to remain a fairly constant population for some time because no new queens are produced and few serious enemies are evident. Also the queens forage independently and therefore the samples should be random. Fig. 2a shows daily catch which measures aerial density directly during the time that insects are active. The initial emergence of wasps from over-wintering sites was missed and the population is, as expected, fairly constant until the end of May when foraging almost ceased. Only the catch for May is used for analysis. In Fig. 2b the individual daily catches, plotted against the maximum temperature for the day, show no regression but indicate a lower threshold. Flight does not take place below about 15?C, but above this temperature there is no evidence that higher temperatures produce more flight. There is no evidence for an upper threshold because temperature did not rise above 22? C. Although this population was chosen because it was thought to be fairly constant in numbers, variation in population level was further eliminated by recording each catch as 1, a positive catch, or 0. The positive catches were then recorded as a percentage of the

104

Temperatureand insectflight

occasions the trap operated, within any temperatureinterval. In this instance, because the occasions are few and the temperatureintervals must be large to obtain a percentage, the result is rather crude (Fig. 3a). It is claimed that this representsa threshold, not a regression. This is not self-evident from the figure because there are so few points, but analogy with the examples shown later makes this conclusion likely.
30-

a
0 10 10?o

?
0 00? 0 0 0 O

?D

'

r 4 4J 92-

? 0, ? ' a o o0 co o

? 0

? OD)

? ? 0 0

e
U 1 0

0 o

0-

o0

CCoCC'

ccocs

o c_o:zD

oo

0 00

00

0o0

510

15 20 MAY

25

305101520 JU NE

10

15 TEMPERATURE

20 ( C)

FiG. 2. (a) Daily (24 h) catches of queen wasps showing the change in populationlevel at the end of May. (b) Crudeflight thresholdobtainedby plottingdailycatch for May againstmaximumtemperature duringthe day.

As already suggested, when population level remains fairly constant, a 24 h catch is equal to the product of the length of flying time and the mean aerial density:
C24

5Tf = kpTf

i.e. a regression equation between C24and Tf the time above the threshold, where kp is a constant related to the level of population.
12 100-.O 0

0 b

~~~~~~~~~~~~~~~~100

80
U

~~~~~~~~~~~~~0
6H

z
Ui

rr

60 Cr

~~~~~~~~~~~~~~~~~

u
0 0

0
0

~~~~~~~~~~~u
0 0

~~~ 20
U
0

2 c
0

0~~~~~~~~~~~~~~~~~~~~~~~~~ ~~~~~~~~~~~~~~~00
00 0 0

10

15 TEMPERATURE

20 (?C)

25

2 No OF

HOURS0

I'2

AT TEMP

> 15 5 ?C

FiG. 3. (a) Quantitativeexpression of the flight threshold for queen wasps obtained by plotting the percentageof occasions when flight occurredagainst maximumtemperature. (b) Regressionof 24 h catch againstthe time availablefor flightper day, i.e. time above the threshold, based on the assumption that population is relatively constant.

Accepting the view that Fig. 3a shows a threshold temperature for flight, flight is not inhibited by temperature above 15.50 C. If flight is inhibited only by temperature, the value Tf is represented by the period that temperatureremainedabove 15.50 C. The regression is plotted in Fig. 3b; the correlation is very highly significant (Table 1) and the

L. R. TAYLOR

105

regression line does not depart significantly from the origin, conforming with expectations. This means that the major factor in the catch is time, although temperature is the factor operating on the insects' behaviour, and that once the temperature has passed the threshold, the aerial insect density is independent of temperature, remaining constant at a mean value of 3-1 wasps per 5 5 h sample of air, i.e. 14-5 queens per 106 ft3 air

(28 320 m3).

Table 2. Data for temperaturethresholddistributions
Temperature
(OC)

Aphisfabae A B

tragopoginis Rhagonychafulva Agrocholalychnidis Amphipyra A B A 4 3 1 3 1 3 7 10 15 16 26 23 18 6 11 13 5 6 1 B 0 0 0 0 0 0 0 1 3 5 5 6 7 2 4 4 1 0 0 A 1 3 5 12 29 29 42 42 71 82 91 127 134 116 114 69 43 25 15 6 6 1 B 0 0 0 0 2 0 2 3 6 13 16 25 27 22 22 20 18 9 6 2 1 0

<1 1-2 2-3 3-4 4-5 5-6 6-7 7-8 8-9 9-10 10-11 11-12 12-13 13-14 14-15 15-16 16-17 17-18 18-19 19-20 20-21 21-22 22-23 23-24 24-25 25-26 26-27 27-28 28-29 29-30 30-31 31-32 32-33 33-34 34-35 35-36

1 1 2 5 12 18 20 24 20 32 44 60 84 68 62 45 29 31 37 28 27 22 23 11 10 1 1 2

0 0 0 0 0 0 1 2 7 20 29 50 58 67 62 44 28 31 37 28 27 22 19 8 8 1 1 2
A=

4 7 3 2 12 21 36 33 23 43 48 51 75 40 28 17 20 22 18 26 17 10 3 4 1

0 0 0 0 0 0 0 1 1 4 9 12 25 14 9 6 7 8 5 6 1 0 0 0 0

No. of times the temperatureoccurred. B = No. of times a catch occurredat this temperature.

Example 2. Aphis fabae Scop. (The black bean aphid) The second species was chosen because it has already been shown, by analysis (Johnson, 1952) and by synthesis (Johnson et al. 1957), that the biggest element in the variation of current aerial density is population level and that this fluctuates violently from hour to hour. In this example there is experimental evidence of the flight period (Tf) measured in half-hourly periods, and use of this replaces the use of catch size, which in Example 1

106

Temperatureand insectflight

is based on the assumption that population level is constant. The available data are 1152 consecutive half-hourly samples of insects and a continuous temperature record. Flight in A. fabae is inhibited by low light intensity as well as by low temperature and this light threshold operates especially in the evening when sunset occurs before temperature falls low. It is necessary to elucidate both light and temperaturethresholds together, for the action of one obscures the other. By a procedure similar to that used for the temperature threshold, the light threshold was obtained, using time as an index of light intensity with which it is very closely correlated. The result is in Fig. 4a, in which an arithmetic probability curve is fitted graphically to the points. From this curve the 50 % point was read off and for the temperature analysis only the hours from 04.30 to 19.30, i.e. above the mean light threshold, were used. The temperature threshold is sought on the hypothesis that a catch of one or more insects is evidence of flight occurring, the size of the catch being irrelevant. Johnson (1952) showed that regression analysis of catch x mean temperature failed. Each halfhourly catch is therefore recorded as positive (one or more insects) or zero and the number of positive catches within each 10 C temperatureinterval is obtained as a percent100-

12.00
'i 80-

18.00

z 600

0 4020

012.00 18.00 G. M.T. 24.00 6 10 14 22 1B TEMPERATURE 26 30 (OC) 34

in Aphisfabae obtainedby plotting FIG. 4. Thresholdfor (a) light and (b) temperature the percentageoccasions that flight occurredagainst the time and the maximumtemperatureat 4 ft (1-2m)duringhalf-hourtrappingperiods,respectively.

age of the sum of positive and zero catches within that interval. This percentage of occasions when flight occurred is plotted against temperature (Fig. 4b) and an arithmetic probability curve fitted graphically; this is the temperature threshold with a mean of 17-50 C, close to the value obtained experimentallyin the laboratory (Johnson & Taylor 1957). If aerial density is determined largely by population level and flight behaviour in relation to light and temperature and these relations are adequately represented by the thresholds in Figs. 4a and 4b, and if the population changes are largely eliminated by recording catches only as 0 or 1, then, the number of half hours on which a catch was obtained should be correlated with the time period between the morning and evening thresholds for light or temperature, whichever operated. This correlation is shown in Fig. Sa, compared with the correlation of catch on time in Fig. 5b. The fitted regression (Fig. Sa), (measured flight period) = 1-5+0-875x (expected flight period in hours), is very highly significant (Table 1), explaining over 70% of the variance. One source of residual variance is doubtless the lower limit of sensitivity of the trap, for the three most divergent points all occurred when the catch was persistently low. Another source is the

L. R. TAYLOR

107

use of only one trap to sample from innumerable microclimates so that considerable errors occur when temperatureremains within the threshold region for several consecutive catch periods, and a third source is the probable interaction between light and temperature within the threshold ranges, i.e. such an interaction as was demonstrated so beautifully for wasps by Gaul (1952). Nevertheless, the sensitivity of the trap is very high; positive catches rise to 100% of possible occasions at most temperaturesabove the threshold. It is this increased sensitivity and the fact that flight period is measured directly, instead of indirectly, that increases in Example 1 to 710 in Example 2, and gives results the explained variance from 40 %o that compare favourably in precision with laboratory experiments. This trap was at vegetation level in a crop of host plants producing the aphids. The aphids were making their initial migratory flight away from the crop and hence the threshold is for take-off rather than continued flight (see later). It is also striking that
1800 16 _
14-

o oS ?
<

16001400b

c] 12 0 1 lO-

I 1200 u <1000 ~~~~~~~~~~u

a
/ 5 o

H8 _ I J 6 C 4 -

> 800-

C] 600-

D
20 o,0-

~~~~~~~~~~01
'
0 o

400-

~~~~~~~~~~2004 0 2 EXPECTED 14 10 12 6 8 FLIGHT PERIOD (h) 16

0 4 2 EXPECTED

8 6 10 12 FLIGHT PERIOD

14 h)

16

FIG. 5. The total daily catch of Aphisfabae gives no regressionwhen plotted against the time available for flight (b) because of population fluctuationseven from hour to hour. When population fluctuationsare eliminatedby plotting the hours during which flight occurred against time available, a very significant regressionappears(a).

take-off is not inhibited by temperaturesup to at least 360 C. This is above the maximum temperature for teneral development (Taylor 1957). Example 3. Rhagonycha fulva (Scop.) (The soldier beetle) The trap sensitivity was so high relative to the population density that Aphis fabae were nearly always caught when both light and temperaturewere above the threshold for of flight, i.e. the whole available flight period is utilized, flight usually occurred on 100%Y possible occasions (Figs. 4a and 4b). In addition, no upper temperature threshold was found for A. fabae up to 360 C. Rhagonychafulva was chosen to illustrate these two points further. R. fulva is not nearly so common as Aphisfabae. Hence the sensitivity of the trap, the same one as used for A. fabae, is much lower for this insect and many half-hour samples were taken when activity was inhibited neither by low light nor temperature but aerial density was nevertheless too low to yield a catch. In all, 181 insects were caught during 816 half-hourly samples in 17 days, an average of only 0-22 insects per sample; the daily totals varied from 2 to 22.

108

Temperatureand insectflight

There is clear evidence of an upper, as well as a lower threshold (Fig. 6). Both thresholds appear to be arithmetic probability distributions; the evidence for the upper threshold occurred mainly on 2 days and more catches might modify its value. The temperature used was the mean for each half-hour period at 1 ft from the ground. On
0 _j
UPPER LOWER

_50-,

uiJ40-,

uJ4

a30:D c 20-

i 10

A 0 4

0~~~~~~~~
0I 6 a 10 12 14

20 16 1a TEMPERATURE

22 (OC)

24

26

2a

30

32

FIG.. 6. The percentage flight occurrence curve for Rhagonychafulva showing both the lower and upper flight thresholdsagainst mean temperature at 1 ft (0 3 m).

most days, flight was plainly inhibited by low temperature in the evening, but, because Rhagonycha fulva has not been found in traps between 22.00 and 02.00 hours, these hours of darkness were omitted from the computing. Between the lower and upper temperature thresholds the percentage occasions that
2412
0 0 -L

T20-

0
0 00

<12

0
0

o6
00 0 0

C ~~~~~~~~~~~~~~~~~~~~~ ~~~~~~~~~~~~~~0
0

110

ff~~~0

0 0

ui

-0

40

2-

a4

4 2 EXPECTED

8 6 FLIGHT

10 PERIOD

12 (h)

14

2 4 EXPECTED

6 8 10 FLIGHT PERIOD

12 (h)

14

FIG. 7. Daily catch of Rhagonychafulva gives no regression(a), but the measuredflight

period gives a regressionwhen the last 3 days (solid dots) are excluded(b).

flight was observed levels off at about 34 %. In other words, only one sample in three has a catch, even when neither light nor temperature are limiting factors. This has a considerable effect on trap accuracy, as can be seen in Figs. 7a and 7b, in which the daily catch and the measured flight period are plotted against the expected flight period. There is no longer any significant correlation. However, if the last 3 days are excluded, i.e. when

L. R.

TAYLOR

109

the population level was at its lowest before disappearingaltogether, a correlation appears which is almost significant (10 % level) for the daily catch and just significant (5 % level) for the expected flying time (Table 1); 30 % of the variance of the expected flying time is explained but only 22 % for the daily catch, showing that the population was not constant. The regression for E.F.P. x M.F.P. passes almost through the origin (yo = 0-21). By comparison with the figures for queen wasps for which the trap sensitivity was even lower, it seems likely that some other factor remains to be found. However, the halfhourly segregation of the catch considerably improves the threshold distributions. Compared with the results for Aphisfabae, the lower sensitivity of the trap lessens the total efficiency of the method and, especially when the sample mean is near 1, the device for removing population fluctuations is much less effective.

Examples 4 and 5. Agrochola lychnidis and Amphipyra tragopoginis (Lepidoptera) The examples dealt with so far have been day-flying insects. Light is demonstrably a limiting factor for some, but there are many possible trapping hours above the light threshold during which flight is limited largely, even entirely, by temperature. For insects that fly by night, the situation is very different. Light is plainly a major factor in determining flight periodicity which may be strikingly different for different species. Factors affecting a flying population of Macrolepidoptera have already been described (Taylor & Carter 1961) and the temperaturethresholds and flight periodicities illustrated for the two night-flying moths that were sufficiently common for full analysis. The method adopted was as follows. Using those hours of the night when flight can occur, each hour's catch was plotted against temperature in a scatter diagram. Catches were then summed in 10 C temperature intervals and a smooth sigmoid curve drawn through the resulting points. A clear graphical demonstration of a threshold emerged with modes at 90 C and 10.50 C for Agrochola lychnidis and Amphipyra tragopoginis respectively (see Taylor & Carter 1961). From the previous discussion it is obvious that this method accepts the implication that the population level remains fairly constant; even the catches from different years are summed. According to the arguments advanced here, a clearer result should emerge if population level is eliminated by the use of percentage flight occurrence. Agrochola lychnidis (Schif.) (The beaded chestnut) Fig. 8a shows the flight periodicity for this moth. Using only the 4 h of most common flight, 16.00-20.00 hours, Fig. 8b gives the percentage flight occurrence for October in the 3 years 1953/54/55. The flight pattern within the hours 16.00-20.00 is simple, and the resulting temperature thresholds are clear and convincing. The lower threshold is at 80 C compared with 90 C obtained when catch size is included (Taylor & Carter 1961). The lower value, 80 C, may be taken to be the threshold above which flight can occur; the higher value, 90 C, to be that above which flight did occur most often. The upper threshold, 16.60 C, is remarkablylow. This may be accounted for by the adaptation of a temperature tolerance to suit the light response, or vice versa, but it may also be an artifact caused by too few trapping occasions. The results presented were from twentyfour successive hourly catches, for each of 30 consecutive days, replicated by four traps, each for 3 years in succession. This demonstrates the difficulty of obtaining adequate material when flight periodicity is narrowly restricted by other factors.

110

Temperatureand insectflight
to

o
ui

LOWER
b

UPPER

5040

>- 40 t uJ30-

ui
4

~~

z
_-/

J30-

w 2.0
1

u20 2 ~~~~~~~~~~~~~0

0~~~~~~~~
0

1~~~~~~~~~~~~~~~~~~I10U.

0 1200 18.00

00.00 G.M .T.

06r.00

2~.00

18

110

TEMPERATURE

12 14 l?C)

16

18

FIG. 8. Using the very restrictedflight period between dotted lines (a), a percentageflight occurrence against curve with lower and upper thresholds(b) is producedby hourly catches of Agrocholalychnidis at 5 ft (1 5 m). mean temperature

100>-80360-

40-

2020

12.00 C] 0

0~~~~~~~0
b b

I 00.00 G.IM.T 06.00 UPPER 12.00

18.00

2
I
uLJ

LOWER

40-

cj30-

'

'

't

0~~2
2 4 6 8 12 10 TEMPERATURE 14 (?C) 16 la 20

88

22

24

shows two tragopoginis FIG.9. Flight periodicityin Amphipyra differentlevels of aerial density(a). Lowerand upperthresholds at 5 ft (1 5 m) are found, of flightagainstmaximumtemperature but the percentage flight curve is complex, unlike previous examples.

L. R. TAYLOR

111

Amphipyra tragopoginis (Linn.) (The mouse) Fig. 9a shows daily flight periodicity and Fig. 9b the percentage flight. Using the hours 19.00-05.00 during the season of flight, 1 Aug.-20 Sept. 1954 and 26 July-30 Sept. 1955, there appear to be two distinct levels of activity; between 12 and 160C and between 17 and 210 C, giving rise to two apparent thresholds, at 9.250 C and 16.50 C; the 9.250 C threshold has a very wide distribution. I have no completely satisfying explanation for this, although it is evident from col. 8, Table 2, that the increase at 16-50 C is not caused by an increase in positive catches above this temperature, but perhaps the explanation should be sought in the interaction between the daily temperature cycle and the form of the flight periodicity curve (Fig. 9a). For the present purpose, the lower threshold is at 9.250 C and an upper threshold, of doubtful validity, is at 21.50 C. DISCUSSION It appears from the examples given, that the lower temperaturethreshold is, in temperate climates, an important climatic factor determining insect flight and that it can be clearly and simply measured by trap catches. There is no doubt that there is also an upper threshold, although it acts less often than the lower in southern England. It is therefore pertinent to consider whether the laboratory work done on insect flight conforms with these results. A basic assumption throughout these analyses has been that, provided the temperature is high enough to allow the insect to generate energy enough to maintain flight, flight occurrence is relatively independent of temperature. This implies that both ability to fly, and willingness, are independent of temperature. The evidence from laboratory experiments is limited to a few species and most of the studies of flight functions in relation to temperature have been concerned with some limited aspect of flight such as wing-beat frequency or amplitude. However, this indicates ability to fly, if not willingness. In a study of the tethered flight of the Douglas Fir beetle (Dendroctonus pseudotsugae Hopk.), Atkins (1960) observed, 'Temperature did not affect the wing-beat amplitude. It seems noteworthy that the wing-beat frequency increased rapidly with temperatureup to 680 to 720 F, the point at which spontaneous flight occurs. Once the optimal temperature for flight was reached, wing-beat frequency increased by only a few cycles per second with an additional rise of 180 F.' It seems likely that 'optimal temperature'in this context is synonymous with 'threshold temperature'as used here. Sotavalta (1947) records wing-beat frequency at different temperatures for fifteen species of insects; four species of Hymenoptera (Apis mellifica L.; Bombus agrorum F.; Vespa vulgaris L.; Absyrtus luteus Hgr.) and one species of Coleoptera (Cantharis sp.) showed no trace of temperature dependence, one species of Lepidoptera (Hemaris fuciformis L.) showed a trivial change of 100%over 300 C, and ten species of Diptera showed increase in wing-beat frequency with increase in temperature. However, it should be noted that over a range of more than 300 C, the average change in frequency was only 38 % of the highest frequency reached; only one species (Musca autumnalis Deg.) doubled its frequency in a range of 320 C. In other words, at the lowest temperature permitting flight, the wing-beat frequency already exceeds half its maximum value in the other nine species (Drosophila melanogaster(Mg.); D. funebris F.; Boreellus terraenovae R-D.; Musca domestica L.; Calliphorasp.; Culicidae spp.; Tipula sp.). Also doubling the wing-beat frequency does not necessarily mean doubling the flight performance. We found that speed of free flight by Aphisfabae Scop., which has a flight threshold of
J.A.E. H

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Temperatureand insectflight

150 C (Cockbain 1961), increases by only about 15% between 17-5and 300 C (unpublished results). Weis-Fogh (1956) working with the locust (Schistocerca gregaria Forskal) tethered on a flight mill, pendulum or balance, concluded that between 25 and 350 C temperature does not affect flight performance nor wing stroke frequency which was chosen because a temperature dependence should have been easy to detect. I conclude that the flight performances of Aphis fabae and Schistocerca gregaria are probably fairly typical; that over the range of temperatures at which an insect can fly, flight ability is affected but little by temperature. It follows that the change from inability to fly to ability to fly occurs abruptly at some fairly critical temperaturewith most insects. The stages in this process have been thoroughly investigated in Aphisfabae by Cockbain (1961), who demonstrated three clearly separate thresholds, for tethered wing-beating (6.50 C), horizontal free flight (130 C), and upward free flight (15? C). However, free flight must be preceded by take-off which has a still higher threshold, 17.30 C (Johnson & Taylor 1957). In practice, therefore, the operative threshold will depend upon whether the temperatureis rising or falling. In a rising temperaturethe take,off threshold must be passed before the insect can fly. In a falling temperature the insect can continue to fly at temperatures below the threshold for take-off until low temperature inhibits wingbeating. In practice, also, one threshold will often be obscured by some other climatic factor such as light. The realization that take-off plays such an important part in flight may have led to the use of the actograph, or to observation of insects confined in a small container, for measuring 'flight activity'. The many attempts to obtain such a measure have met with little success. The difficulty is in deciding which flight function to measure and how to interpret it. For example Nicholson (1934) recorded the number of flights per blowfly per minute in a 2 in. diam. tube or 200 cm3 beaker, so that take-off was immediately followed by forced landing. It is evident that what was measured was largely forced take-off and re-takeoff. This can rarely happen in nature; once the take-off threshold temperature is exceeded, factors other than temperatureare likely to play a large part in determining alighting and hence the regular sequence of take-off and alighting, which is enforced in the inspection tube, is unlikely to occur in the open. Also, with flights not restrictedto 2 in., the relevant function of temperatureis its effect on continued flight after take-off. Experiments of this kind, therefore, investigate some complex sequence of physical limitations and behaviour patterns with a response curve that rises to a peak and then falls slowly. Observations of caged insects are valid as a measure of activity in a general sense provided the function measured is the percentage of the population moving at any instant, and in this sense give a measure of willingness to move. The cage imparts no restriction on crawling, etc. If flight activity is assumed to bear some relation to activity in general, as Nicholson (1934) suggests, such observations are relevant. Nicholson measured the percentage of insects active at different temperatures in four species of blowfly (Lucilia cuprina Wied., L. sericata Mg., Chrysomyiarufifacies Macq. and Calliphora stygia Fabr.) and of each species about 70 %of flies were active over a range of 200 C at constant temperatures; with continually rising temperatures the range was increased to over 250 C, i.e. a flat-topped response curve. Gunn & Hopf (1941), observing the percentage of the flightless beetle Ptinus tectus Boie. active in a dish at different constant and varying temperatures, concluded that between 15 and 350 C percentage activity changes little in any of the temperature conditions used. The levels of activity differedwith rate and direction of change in temperature but the temperature at which activity commenced differed less (Fig. 10).

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Mellanby (1939) was unable to change the flight threshold of Lucilia and Calliphoraby subjecting them to different temperatures before flight and concluded that Lucilia could fly at 140C whatever conditions it had previously sustained, and again that Ldcilia and Calliphora can fly when their metabolic rates reach a high enough level, and that the 'position of the temperature at which their metabolism reaches that level appears to be fixed'. He goes on to say that there is only one really satisfactory method of discovering the threshold temperature for spontaneous movement, 'that is by observing the behaviour of the insect under natural conditions in its normal habit'. This is precisely what the trap does objectively, but it is none the less important to verify the conclusions, where possible, in the laboratory. From the laboratory work quoted, which seems to be representative, I conclude that the percentage of insects moving, as distinct from speed of movement, is relatively independent of temperatureover a wide range; that the thresholds and levels of movement may vary with rates and directions of changes in temperature;
100-

80-

60

40-

20-

0 0 5 10 20 15 TEMPERATURE 25 (%) 30 35 40

activitycurvesfor Ptinustectus(afterGunn FIG. 10. Percentage & Hopf 1941)show lower and upperthresholdswith wide range at which activity is not much affected of median temperatures affects the level Rate of change of temperature by temperature. of percentageactivity considerablybut the thresholdpositions constant;2, risingfast; 3, rising are affectedless: 1, temperature slowly, the rebound is not accounted for; 4, falling slowly.

that these thresholds are much more rigidly fixed for flight than for other movements and that this is probably associated with the rather complex sequence of actions involved in flight. Of these the one requiring most nervous co-ordination and phsyical energy is take-off, which is the first act of flight and has the highest threshold. As mentioned earlier, the take-off threshold for Aphisfabae in the open is complicated by rapid population changes, but since the most complete data are for this species, I have used it to illustrate the sequence of thresholds involved in flight (Fig. 11). The thresholds are not spot temperatures as may appear where material is selected to lessen variability. The threshold distributions in the laboratory include individual differences in response. In the field these differences are supplemented by variations in the microclimate to which the individuals have been subjected and the distributions may be wider (see Fig. 11). Apart from this, the distribution obtained by differentiation from the integral, sigmoid, curve of flight frequency, should correspond with the laboratory

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Temperatureand insectflight

distribution for the same function. A minor point of interest here, the meaning of which is not clear, is that all distributions are arithmetic probabilities, i.e. are symmetrical, except that for take-off (Johnson & Taylor 1957). This emphasizes a final point: whereas there is no doubt about the meaning of tempera-

z
002

Z~~~~~~~~~~~~~

,/~~~~~~ / ~~*
100-

6u 0'

zi
u0/

U~~
20

10
/

12

r
0 5

10~~Tl

1 20 TEMPERATURE

25 IC0)

30

35

FIG. 11. Percentage flight occurrence curves and the differential temperature thresholds for Aphis fabae: 1, horizontal or upward; 2, upward free flight in the laboratory (Cockbain 1961); 3, take-off in the laboratory (Johnson & Taylor 1957); 4, migratory flight immediately after leaving productive host in the field. There is no flight below 100 C and no change in percentage activity between 20 and 350 C. The upper thresholds have

not yet been found.

Table 3. Temperaturethreshold distributionsfrom field data; obtained graphically from percentage occurrenceplotted as arithmeticprobabilities
Threshold (?C) Lower Upper
-,

Species
Aphis fabae

Temperature
record r4 ft (1-2m) max. 4 ft (1-2m) mean L1ft (0-3 m) mean r4ft (1 2m) max. 4 ft (1-2 m) mean 1 ft(03m)mean 5 ft (15 m) mean Mean 17-5 17-0 15-0 18-2 17-9 16-4 80 9.1 95 % limit ?2-4 +2-4 ?3-8 +3-1 ?4-5 ?23 ?1-9 ?26 Mean <36-0 <35-0 <31-0 27-9 27-6 25-6 17-4 21-4

95 % limit

Rhagonycha fulva Agrochola lychnidis

?4-1 ?1-6 ?1-5 ?07 ?1-3

Amphipyra tragopoginis 5 ft (1i5 m) mean

tures quoted in laboratory experiments, temperatures in the open depend on where and how they are measured (see Table 3). If the field observations are to correspond with laboratory results, the temperature should be that of the insects, and this is not always easy to obtain especially in sunshine. The field temperatures chosen must therefore be a

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115

balance between what the insect experiences and what is reproducible, either in the laboratory or on another occasion. For this purpose the air temperaturemeasured where the insects are being trapped is probably the most useful at least for small insects whose body temperature is unlikely to differ much from air temperature. With large insects, such as hawk moths, the difference between body and air temperature may be 8 or 9? C (Church 1960), yet if the traps effectively measure aerial density, thresholds measured in terms of the air temperatureat the trap have a real ecological meaning, whatever mechanisms of heating are involved and whatever the internal temperature of the insect may be. The trap will not, however, distinguish differencesin behaviour, for example gliding from true flight, and where these have different thresholds, observation is needed to interpret trap catches.
100 ,0

80

80~~~~~~~~~~~

0
o o

'o,
0

60~~~~~~~~~~~~
-640 -O oo

o/

LLIJ,

z Z U

1: 20

r20~~~~~~~~~~ J ,'~~~~~~~9
0 o ,

ooooo

10 20 TEMPERATURE

30 (?C)

35

FIG. 12. Percentageflight occurrencefor a hypotheticalheterogeneous populationconsisting of Aphis fabae, Rhagonycha fulva, Agrocholalychnidisand Amphipyra tragopoginis; data from Table 2. The separate thresholds,so clearly illustratedfor individual species,become mergedinto a population with a response curve more suited to regressionanalysis. The use of total catch instead of percentage flight occurrence would give a similarresult.

There is some evidence of significant regressions of numbers of a single species of insect against temperature. Much of this evidence comes from the extensive work on the tsetse fly and this is most clearly represented by Vanderplank's (1948) results with Glossina pallidipes Austen. Dividing his material into humidity groups, Vanderplank obtained significant regressions of catch x temperature at each humidity, the regression changing from positive at saturation deficits below 25 mb to negative in drier air. However, these catches, like most in tsetse work, are of number of flies biting; in this instance tethered oxen. It is therefore not certain that only flight activity of the flies is concerned; the response to the bait, the attractiveness of the bait, or the transmission of the scent of the bait might vary and influence the catches. The regression relation may be regarded merely as a statistical convenience, approximating to a small part of a wide threshold response, and may sometimes give a good fit

116

Temperatureand insectflight

(see Pinchin & Anderson 1936). There is, however, a more fundamental biological difference between the regression and threshold methods which imply different physiological responses to climatic factors. It is difficult to visualize the behaviour of individuals that would lead to a regression response in a monospecific population; in contrast the threshhold is a feasible functional response based on the observed behaviour of individuals. It is most intelligible in terms of single individuals and the response of a population of a single species is deduced from this, as is permissible because the individuals act independently in this respect. Accepting this view, the regression response becomes intelligible as the summation of the thresholds of different species at differenttemperatures, i.e. such multispecificpopulations as those analysed by Williams. Fig. 12 shows the percentage response of a hypothetical population comprising the samples of four species analysed earlier. The series of absolute temperaturethresholds at which activity is released in differentspecies is replaced by a continuously rising response, very suitable for regression treatment, which redirects attention to the rate of change of total heterogeneous aerial populations as temperature changes. A most interesting and striking result comes from the extensive investigation by Hawkes (1961) into factors affecting the density of the fly Anisopusfenestralis Scop. in and over sewage filter beds. Taking separate wind-speed groups, Hawkes shows a consistent positive regression of the deviation from a running mean of the log insect density against the deviation of temperature, such that the catch is doubled by a rise of 1-20 C. The population density of Anisopus within the limited environment of the filter beds is not, however, constant and may fluctuate in response to temperaturein the reciprocating way implied by regression analysis because of the limited population. Thus population changes may be responsible for these regressions; if subsequent work shows that they are not, a quite different mechanism of flight response to temperature than that suggested here will have been found.

ACKNOWLEDGMENTS It is a pleasure to thank Mr J. P. Spradbery for his determination of the wasps, and Mr M. J. R. Healy for a typically penetrating criticism of the manuscript.

SUMMARY 1. The number of insects in free flight depends upon the population density and the amount of activity. Both are affected by climate, especially temperature. 2. Population changes can be largely eliminated from trap catches by classifying catches as unity or zero, provided the trap is sensitive enough. 3. Analysis of several aerial populations of single species shows that temperature acts as a threshold above which flight is uninhibited. 4. Consequently the time spent at temperatures above the threshold has more effect than mean temperature on the size of daily trap catches. 5. Field measurements of temperature threshold analysed in this way are as accurate as, and strictly comparable with, the results of laboratory experiments. 6. Regression analysis is more appropriate to multispecific populations.

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REFERENCES
Atkins,M. D. (1960). A study of the flight of the Douglas Fir beetle Dendroctonus pseudotsugae Hopk. (Coleoptera: Scolytidae).II. Flight movements. Canad.Ent. 92, 941-54. N. S. (1960).Heat loss and the body temperature Church, of flyinginsects.II. Heat conductionwithinthe body and its loss by radiationand convection. J. Exp. Biol. 37, 186-212. Cockbain,A. J. (1961). Low temperature thresholdsfor flight in Aphisfabae Scop. Ent. Exp. Appl. 4, 211-19. Gaul, A. T. (1952). The awakeningand diurnalflight activity of vespinewasps. Proc. R. Ent. Soc. Lond. A, 27, 33-8. Gunn,D. L. &Hopf,H. S. (1941).The biologyand behaviourof PtinustectusBoie. (Coleoptera:Ptinidae), a pest of stored products. II. The amount of locomotory activity in relation to experimentaland previous temperatures.J. Exp. Biol. 18, 278-89. Hawkes, H. A. (1961). Fluctuationsin the aerial density of Anisopus fenestralisScop. (Diptera)above sewage bacteriabeds. Ann. Appl. Biol. 49, 66-76. Johnson,C. G. (1952). The changingnumbersof Aphisfabae Scop., flying at crop level, in relation to currentweatherand to the population on the crop. Ann. Appl. Biol. 39, 525-47. Johnson,C. G. & Taylor,L. R. (1955). The developmentof large suction traps for airborneinsects.Ann. Appl.Biol. 43, 51-62. Johnson,C. G. & Taylor,L. R. (1957). Periodismand energysummationwith specialreferenceto flight rhythmsin aphids. J. Exp. Biol. 34, 209-21. Johnson,C. G., Taylor,L. R. & Haine, E. (1957). The analysisand reconstruction of diurnalflightcurves in alienicolaeof Aphisfabae Scop. Ann. Appl. Biol. 45, 682-701. Kloet, G. S. & Hincks, W. D. (1945). A CheckList of BritishInsects. Stockport. Mellanby,K. (1939). Low temperature and insect activity. Proc. Roy. Soc. B, 127, 473-87. Nicholson,A. J. (1934). The influenceof temperature on the activity of sheep blowflies. Bull. Ent. Res.
25, 85-99.

Pinchin,R. D. & Anderson, J. (1936). On the nocturnalactivity of Tipulinae(Diptera) as measuredby a light trap. (2) The influence of temperature,cloud and moonlight on the numbers of insects captured. Proc. R. Ent. Soc. Lond. A, 11, 75-8. Sotavalta,0. (1947). The flight-tone(wing-strokefrequency)of insects. Acta Ent. Fenn. 4, 1-117. Taylor,L. R. (1951). An improvedsuction trap for insects. Ann. Appl. Biol. 38, 582-91. Taylor,L. R. (1957). Temperature relationsof teneraldevelopmentand behaviourin Aphisfabae Scop. J. Exp. Biol. 34, 189-208. Taylor,L. R. & Carter,C. I. (1961). The analysisof numbersand distributionin an aerialpopulation of Macrolepidoptera.Trans.R. Ent. Soc. Lond. 113, 369-86. F. L. (1948). Studies of the behaviour of the tsetse fly, Glossinapallidipes, in the field: Vanderplank, Influenceof climaticfactors on activity. J. Anim.Ecol. 17, 245-60. Weis-Fogh,T. (1956). Biology and physics of locust flight. II. Flight performanceof the desert locust (Schistocerca gregaria). Phil. Trans.B, 239, 459-510. Williams,C. B. (1940). The analysisof four years capturesof insects in a light trap. Part 2. The effect of weatherconditions on insect activity; and the estimation and forecastingof changes in the insect population. Trans.R. Ent. Soc. Lond. 90, 227-306. Williams,C. B. (1961). Studiesin the effectof weatherconditionson the activityand abundanceof insect populations. Phil. Trans.B, 244, 331-78. Williams,C. B. & Osman,M. F. H. (1960). A new approachto the problemof the optimumtemperature for insect activity. J. Anim.Ecol. 29, 187-90.