i 8 7

THE HUMIDITY REACTIONS OF THE AFRICANMIGRATORY LOCUST, LOCUSTA MIGRA-

TORIA MIGRATORIOIDES R. & F.,GREGARIOUS PHASE

BY JOHN S. KENNEDY

From the Zoology Department, University of Birmingham

(Received 2 October 1936)

(With Four Text-figures)

I. INTRODUCTION

THERE is some field evidence that the distribution of locusts is related to humidityas well as to temperature. Lean (1931) has suggested that air humidity limits thearea of dispersal of Locusta swarms, and similar conclusions have been drawn bySmee (1936) from the behaviour of the Red Locust (Nomadacris septemfasciata).Bodenheimer (on Schistocerca, 1930) and Hamilton (on Locusta, Scfnstocerca, andNomadacris, 1936) in an extensive series of laboratory experiments, have shown thatair humidity is an important factor in development and sexual maturation. Of thefew laboratory experiments on the reactions of animals to air humidity only thoseof Rubtzov (1935) and Key (1936), discussed below, have been done on locusts. Aninvestigation has therefore been carried out of the reactions of Locusta to airhumidity as a stimulus.

II. MATERIAL

The locusts used for these experiments were all of the gregarious phase. Stockswere obtained from time to time from the Locust Laboratory of the Imperial In-stitute of Entomology, British Museum (Natural History), London, and had origin-ally been sent to the Institute from the Sudan and Kenya. They were bred in thislaboratory in cages similar to those described by Hamilton (1936), and in larger ones,under the conditions of temperature and humidity prescribed by that author. Itmust be emphasized that the values given below for cage humidity have onlyrelative meaning, since in all cases the air was almost saturated near the grasssupplied as food, while over the heaters it was very dry. The hygrometer was placedapproximately midway between the grass and the heater, with the sensitive paperof the hygrometer an inch or two from the floor. Humidity control was effected byvarying the amount of moisture in the sand on the floor of the cage, and by varyingthe ventilation.

JOHN S. KENNEDY

III. EXPERIMENTS WITH THE ALTERNATIVE CHAMBER

Under standard conditions

The alternative chamber, as described by Gunn & Kennedy (1936), was usedfor finding out whether or not locusts have a humidity preference. The animalscould walk in this chamber, but the roof was too low to allow either flying orhopping. Under illumination of 65 metre-candles the locusts were too active forposition readings to be made. In order to reduce the activity a sheet of brown paperwas placed on the lid which kept the intensity of illumination at 5 metre-candles, andreduced the locusts' activity sufficiently for experimental purposes. All the experi-ments except a few mentioned below were carried out in a room maintained attemperatures between 29 and 320 C.

Table I

Stage

I8t2nd3rd4th5th

Sexuallymatureadult S

Sexuallymatureadult $

Diameterof

chamberusedcm.

)

J1 "

30

J

Averagedifferencebetweenhumidityextremes

% R.H.

48

60

70

Range ofvariationof lowest

humidities% R.H.

I5-5O

15-45

8-40

Range ofvariationof highesthumidities

% R.H.

(76-85

187-92 {

(

93-96 -j

I

Read-ings in

dryhalfD

297275370

261356

312

2 2 2

Read-ings onmid-line

262838

3059

78

87

Read-ings in

wethalfW

979792

6975

90

IOI

RatioDIW

3 02 93 6

3-84-8

3 6

2 - 2

Ten animals were placed in the chamber and time allowed for the gradient tosettle down again. Every 20 min. a record was made of the numbers of animals inthe drier hah0, in the moister hah0, and on the middle line. After each reading theanimals were stirred by means of a bright light until eight or more were attractedinto one half. The animals were stirred to the moister and to the drier halvesalternately. In one set of experiments, after five readings the chamber was turnedthrough 1800 as a control of stimuli arising externally to the chamber. At the sametime the hygrometers were interchanged. Another five readings were then taken,making a total of ten readings and 100 positions. In another set of experiments themore carefully controlled experimental method described by Gunn (1937) was used,whereby a total of 200 positions was recorded. The results from the two sets weresimilar. In both methods each hygrometer records the humidity in each side of thechamber in turn, and the mean of the two humidity differences was the value used.

The results obtained with all stadia of Locusta are given in Table I, and it willbe seen that in all cases there is a preference for dry air.

Humidity Reactions of the African Migratory Locust 189

A comparable set of experiments on immature adults was not done in thisseries, but similar experiments showed that both male and female immature adultshave a preference for dry air (e.g. p. 192).

The strength of the reaction under these circumstances is conveniently expressedas the number of animals in the drier side divided by the number in the wetter side(ratio D/W; "intensity of reaction" of Gunn, 1937). The average percentage on themiddle line for all stadia was 11 (minimum 4, maximum 16 for hoppers and adultmales, 24 for adult females).

Control experiments carried out in exactly the same way (200 positions) inchambers with uniform humidities, gave an average ratio D/W of o-98 + o-oi(min. 075, max. 1-63). The possibility that the results were due to the locustsreacting positively to the sulphuric acid itself rather than to the low humidity, was

Table II

Humidityrange covered

% R.H.

10-41IO-2I

O-2O8-228-217-317-l8

Readingsin dry half

D

n o469754SS

1 1 4

96

Readingson mid-line

422 04817133445

Readingsin wet half

W

4934SS29325257

RatioD/W

2-2i-4i-8i-81 72-21 7

excluded by experiments in which saturated solutions of such salts as potassiumtartrate, potassium chloride, and ammonium nitrate were used instead of the acid(Buxton & Mellanby, 1934). The use of various stirring methods showed that thealternate method described above does not cause a bias simulating a preference.This was confirmed in the experiments where the aktograph was used as an alter-native chamber, and no stirring whatever was done (see below). The differencesbetween the ratios D/W for different stadia must be disregarded, since it is impos-sible to allow for variations in gregarious behaviour with different stadia of differentsizes in different sized chambers.

The results show a definite, if not very strong, preference for the drier half ofthe chamber. The experiments listed in Table I were designed simply in order toestablish the existence of a reaction to air humidity. As was pointed out by Gunn &Kennedy (1936), it is not possible to say to what humidity difference the animalsare reacting in the alternative chamber, especially when maximum differences of asmuch as 50 per cent are available. In particular, the results do not reveal whetherthe locusts have a preferred ("optimum") region of the humidity range, since sucha region may be included in the dry half of the wide range offered in the chamber.In a series of experiments principally on 5th stage hoppers, in alternative chambersin which smaller differences of humidity were provided, a majority of hoppers wasalways found in the drier half of the chamber, irrespective of where the limitinghumidities concerned lay in the humidity range:

190 JOHN S. KENNEDY

The above figures (Table II) of single experiments on 5th stage hoppersshow that the dry preference persists even in the driest portion of the humidityrange which could be reached experimentally. A ratio D/W of 1-4 is actually lessthan the highest value (i-6, see p. 189) obtained in the no-difference controls, butas none of the above experiments gave a negative result the ratio i*4,is probably moresignificant than the control suggests. As will be seen below, the magnitude of thehumidity difference available in the chamber is an important factor in determiningthe value of D/W. Since the humidity differences are much greater in Table Ithan in Table II the smaller values of D/W shown in Table II cannot be ascribedsimply to the greater dryness of the air.

Variation in the reaction, even in experiments with roughly equal humiditydifferences and in about the same region of the humidity range, is, as indicatedabove, very great. One cause of the variation in the ratio D/W was undoubtedly thewide variation in the level of activity of the locusts (Key, 1936), since it was aproperty of the experimental technique employed (stirring alternately to wet anddry halves) that the lower the animals' activity, the nearer the ratio D/W approachedunity. Experiments with various humidity differences in different parts of therange showed no marked dependence of the ratio D/W on the region of the humidityrange, such as Gunn (1937) has found for PorcelUo scaber. For instance, whenextremes of humidity 18-28 per cent R.H. apart (mean 23 per cent) were set up inthe chambers, ratios D/Woi 3-6 and 2-2 were obtained below 40 per cent R.H., ratiosof 4-0 and 2-0 in the middle humidity region, and of 2-1 and 3-2 when both extremeswere above 60 per cent R.H. A series of alternative chamber experiments with singleimmature adult males (illumination 65 metre-candles) did, however, give a highervalue of D/W in the moist portion of the range (above 64 per cent R.H.) than in thedry (below 37 per cent R.H.). Although the difference was not statistically significant,it suggests that a larger number of experiments with humidity ranges of equallength might yield a significantly smaller value of D/ W in the moist region than inthe dry. On the other hand, Fig. 1 shows that the ratio D/W is roughly correlatedwith the extreme difference of humidity available. Fig. 1 also shows that when lessthan 20 per cent R.H. difference is available in the chamber, Z)/PFapproaches the valuesobtained in the control experiments. This 20 per cent difference in the chambersused for 5th stage hoppers represents an average gradient of slightly less than 1 percent R.H. per cm.

Effect of low humidity in cages

Experiments were done to find the effect of previous humidity conditions onthe humidity preference. Fifth stage hoppers were fed, but kept up to 10 days incages in which the humidity (measured as described on p. 187) varied between 22 and32 per cent R.H. One set of hoppers was tested on the 1st and 2nd days, and two setsof hoppers on the 3rd, 6th, 7th, 8th, 9th and 10th days after they had been placedin the dry air cage, making a total of fourteen experiments and 1177 position readings(excluding mid-line readings). The average ratio D/W was 3-8 (i-4-9'O), comparedwith 4-8 (2'4-9'Q) for similar animals kept at 45-80 per cent R.H.

Humidity Reactions of the African Migratory Locust 19 J

Only two sets of experiments have been done on hoppers kept both in dry cagesand without food. On the 4th day of such treatment the hoppers became moribund.With one set of 5th stage hoppers kept in cages at 15 to 18 per cent R.H. a ratioDjW of 2'5 was obtained on the ist day (hoppers placed in dry cage on previousevening), of i-6 on the 2nd day, and of 1-7 on the 3rd day. The second set ofhoppers, kept in cages between 24 and 27 per cent R.H., gave a ratio of 14-0 on theist, 3-4 on the 2nd, and 17 on the 3rd day.

5-0

4-0

RatioDry readingsWet readings

2-0

1-0

O O O O O O

00 o° "!>

QOO 8 0

— •<%

0 20 40 60 80

Per cent relative humidity difference available in chamberFig. 1. Intensity of reaction in relation to difference of humidity available in alternative chambers,ist and 5th instar hoppers and adult males. Broken line represents highest value obtained in controlexperiments. A ratio D/W of i-o is equivalent to no reaction.

For the technical reason given on p. 190, the changes which the ratio DjWundergoes in the above figures do not necessarily represent a diminution of drypreference, when the level of activity is declining. It can therefore be concludedthat keeping hoppers in drier cages for a few days, at least, does not destroy the dryair preference, but the possibility remains that it reduces the intensity of thatpreference. The detailed results do not demonstrate a reduction of intensity ofreaction, but at the same time they do not eliminate such a possibility.

192 J O H N S. KENNEDY

Effect of brighter illumination combined with lower temperature

Experiments were carried out with full range chambers (average difference ofhumidity 60 per cent R.H.) in much cooler conditions in a north light in a room thetemperature of which averaged 20-0° C. (i8-6-23-6° C). With a total of 429 positionreadings with 5th stage hoppers, an average ratio D/W of 5-4 (2-9-8-7) was ob-tained, and with a total of 437 readings for immature male adults, a ratio of 6-9(3•2-8-8). That is, the reaction is still present under conditions of temperature andillumination different from those in which the bulk of the experiments were done.

IV. MECHANISM OF THE REACTION

Fifth stage hoppers were placed singly in the aktograph (Gunn & Kennedy,1936) in alternately moist and dry air for 1 hour each, under illumination of 5 metre-candles. The basal level of activity varied a great deal from animal to animal, so thatthe results are purely relative. Fig. 2 shows one case where a very clear reaction wasobtained and one which was doubtful. On the whole, the animals were more activein moist air than in dry. In twenty-two cases in which the animal was tested firstin dry air and then in moist, there was no change in six cases, and an increase insixteen cases. In twenty-five cases in which the animal was tested first in moist airand then in dry, there was a decrease of activity in sixteen cases, and no change innine cases. Experiments in which the activity did not change by more than 50 percent were included in the neutral class. Moist air tends therefore to make thehoppers more active, and dry air to decrease their activity; they exhibit an hygro-kinesis. On the other hand, when the exposure is extended to 23 hours, activitybears no constant relation to the humidity of the air—i.e. the hygrokinesis does notlast for long periods.

When the aktograph was used as an alternative chamber, that is, when one halfof the chamber was kept moist and the other half kept dry, five out of eight recordsshowed that while the locust did not always stay for long periods in one half, theinactive periods occurred predominantly in the drier half during a whole day (Fig. 3).The remaining three records-were ambiguous. Thus the continuance of the hygro-kinesis of Locusta, unlike that of Porcellio, requires occasional exposures to adifferent humidity from that preferred.

Single individuals were observed in alternative chambers and their tracks drawn(Fig. 4). There was no evidence of a clear-cut avoiding reaction as a component ofthe humidity reaction. Examination of Fig. 3 shows that on many excursions awayfrom the drier end of the aktograph, the locust does in fact return into the dry halfwithout going right into the moist end. This was also observed in the alternativechamber, but the reaction by which it is effected is difficult to allot to any of therecognized categories of behaviour (Fraenkel, 1931). When passing from the drierhalf towards the moist end of the chamber, the animal was often seen to turn aside,and veer round until it returned into the dry region again. Sometimes, after turning,it walked along or parallel to the middle line; with some individuals this, perhapshygrophobotactic, reaction occurred very often, while with others it did not occur

Humidity Reactions of the African Migratory Locust

Fig. 2. i-hour aktograph records of 5th instar hoppers, a, good reaction; b, doubtful reaction.

3.30.p.m.16.U.3S

5thstage '" 'hoppercl-Zg.from 85per cent R.H.

Fig. 3. 23-hour record of a sth instar hopper in the aktograph used as an alternative chamber. Thecontinuous fall is due to distillation of water from the moist to the dry side. Animal in moist sideduring upper halves of strokes, in dry side during lower halves of strokes.

Dry Moist

Fig. 4. Path followed for about 8 min. by the head of an adult male Locusta in an alternative chamber.Broken line represents boundary between the two sets of humidity controlling dishes, s., start;/.,finish; tt., turning reactions. It will be noticed that in the middle of the chamber the animal usuallypasses uninterruptedly from the moist into the dry side, but executes more or less sharp turns whenmoving from dry to moist.

Humidity Reactions of the African Migratory Locust 195

at all. Progress from the moist to the dry was, on the contrary, usually uninter-rupted.

Attempts were made by various means to evoke a turning reaction throughasymmetrical stimulation of single individuals. Small dishes of water and sulphuricacid were placed under a perforated floor under the two sides of the animal. Cur-rents of moist and dry air were allowed to play on opposite parts such as antennae,palps, thoracic spiracles, and abdomen. No evidence of orientation under theinfluence of these stimuli has so far been obtained.

V. DISCUSSIONIt has been stated above that the least gradient in an alternative chamber to

which animals show a good reaction is about 1 per cent R.H. per cm. The actualhumidity difference between symmetrical humidity receptors (if they exist) istherefore very small. This fact, taken in conjunction with the negative results fromthe experiments where much greater humidity differences were applied to oppositesides of the animal (p. 195), makes it very unlikely that the reaction is tropotactic.The reaction appears rather to resemble the behaviour of planarians (Dendro-coelum lacteum) in a gradient of light intensity (Ullyott, 1936). On passing into aregion of higher light intensity, these animals tend to change direction more fre-quently than before, but the rate of change of direction falls off again owing toadaptation if no further increase of intensity is encountered. This kind of behaviourleads the planarians to collect in the darker end of the gradient. The turning reactionof the locust has not been investigated in the light of these results but it will benoted that the rate of change of direction is greatest where the humidity gradientis steepest (Fig. 4) and that adaptation occurs in the hygrokinesis (p. 192).

With regard to the work of other authors, Rubtzov (1935) described an experi-ment in which the preferred temperature of a locust, Chortkippus albomarginatus,was raised by drying the air at the cool end of the temperature gradient and mois-tening the air at the warm end. The absence of any measurements of the actualhumidities in this experiment makes reliable intepretation impossible, and the pos-sibility that in these very experiments the locusts are actually preferring drier air isnot excluded. Key (1936) conducted experiments on the locomotory activity ofLocusta in relation to air humidity by methods very different from mine. Hisanimals were reared either in very wet or in very dry conditions, while mine werereared at 50—80 per cent R.H. In the only experiments which appear capable ofcomparison with mine, namely some of those in which the animals were reared invery wet conditions, he found that 3rd, 4th and 5th stage hoppers were moreactive in dry air than in wet, the opposite of my result. No explanation of thiscontradiction is apparent to me, but it may be said that when analysed in the sameway as his results, my aktograph results show a much larger difference betweenthe activity levels in the two humidity conditions than he obtains.

The fact that in all the experiments described above the locusts show a prefer-ence for dry air, makes it almost impossible to draw conclusions from them havingany bearing upon the available field observations. The condition of high tempera-

196 JOHN S. KENNEDY

ture combined with low illumination may seldom be encountered by locusts in thefield, but the experiments at 200 C. in daylight showed an even stronger preferencefor dry air, so that the reaction is not dependent on the former combination offactors. Yet Rubtzov (1935), for instance, writes: "Although the Acrididae aregenerally xerophytic animals, their second and third stage larvae invariably movetowards higher humidity, and congregate there in dense bands." Hamilton (1936)has shown that the optimum conditions for the development of Locusta are between60 and 75 per cent R.H. Lean (1931) found no breeding in the field below 40 orabove 80 per cent R.H. Thus the low humidity preferred by locusts in my experi-ments is not the optimum humidity for development, maturation, and breeding.

With regard to the migration and dispersal of swarms, Lean (1931) observedduring an invasion of Nigeria by Locusta that the swarms were to be seen onlybetween the 40 and 85 per cent lines of equal relative humidity throughout theinfestation. Similarly, Smee (1936) found that the circling flights of swarms of theRed Locust (Nomadacris septemfasciata) tended to change into flights in one direc-tion, which carried the swarms out of the locality in question, whenever the tem-perature rose above 270 C. and the humidity fell below 60 per cent R.H. It appearsfrom his observations that humidity is a rather more important influence thantemperature.

Immediate application of such results as those obtained in the course of thiswork could not be expected. The prevention of hopping and flying, the low illumin-ation, and the very small distances involved in the experiments, render them in-applicable to the problems of locust distribution and migration. The reaction is inany case weak compared with that of Porcellio (Gunn, 1937), and the ease with whichit may be overcome by an opposing light stimulus (e.g. by the stirring in thealternative chamber experiments) emphasizes this point. According to Fraenkel(1929) and Strelnikov (1936), temperature is the dominating factor in the diurnalbehaviour of locusts. Humidity is ecologically inseparable from temperature, so thatthe reaction may play at any rate some part in diurnal activity.

The apparent contradiction between the results of this work and the fieldobservations will only be resolved by a careful study of physical factors in relationto locusts in the field.

VI. SUMMARY

1. Under the conditions of the experiments described, Locusta migratoriavngratorioid.es shows a preference for dry air in all parts of the humidity range,although dry air is by no means optimal for development, maturation, and breeding.

2. The strength of the reaction is correlated with the magnitude of the humiditydifference available, but appears to be little dependent on the region of the humidityrange.

3. The mechanism of the reaction is hygrokinetic and possibly hygrophobotacticas well, but probably not hygrotropotactic.

This work was carried out with the aid of a grant from the Imperial Institute ofEntomology in the Department of Zoology, University of Birmingham. I have to

Humidity Reactions of the African Migratory Locust 197

thank the members of that Department for the interested and helpful atmospherewhich I found there; in particular, my thanks are due to Prof. H. Munro Fox forhis hospitality and for a considerable amount of apparatus, and to Dr D. L. Gunnfor unfailing help and advice. Acknowledgements are also due to Dr B. P. Uvarovfor his constant encouragement and for originally suggesting the work, and to DrA. G. Hamilton for supplies of locusts and for technical advice on their culture.

REFERENCES

BODENHEIMER, F. S. (1930). Studien sur Epidemiologie, Oekologie und Phytiologie der afrikanischenWanderheuschrecke, Schistocerca gregaria Forsk. Berlin.

BUXTON, P. A. & MBLLANBY, K. (1934). Bull. ent. Res. 25, 171-5.FRABNKKL, G. (1929). Biol. Zbl. 49, 675-80.

(1931). Biol. Rev. 6, 37-87.GUNN, D. L. (1937). J. exp. Biol. 14, 178-86.GUNN, D. L. & KENNEDY, J. S. (1936). J. exp. Biol. 13, 450-9.HAMILTON, A. G. (1936). Trans, ent. Soc. Land. 85, 1-60.KEY, K. H. L. (1936). Bull. ent..Res. 27, 399-422.LEAN, O. B. (1931). Bull. ent. Res. 22, 551-69.RUBTZOV, I. A. (1935). Zasch. Rast. Vredit. 3, 33-8.SMEB, C. (1936). Bull. ent. Res. 27, 15-35.STRELNIKOV, I. D. (1936). Tran. Inst. zool. Acad. Set., U.R.S.S., 2, 637-733.ULLYOTT, P. (1936). J. exp. Biol. 13, 265-78.

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