The behaviour-modifying effect of chlordimeform and endosulfan on the adult whitefly Bemisia tabaci (Genn.) which attacks cotton in the Sudan

CROP PROTECTION

(1986) 5 (5), 341-347

The behaviour-modXying effect of chlordimeform and endosulfan on the adult whitefly Bern&&-z tabaci (Genn.) which attacks cotton in the Sudan S. UK AND V. DITTRICH

Agricultural

Division,

Ciba-Geigy Lt4 Basel, Switzerland

Chlordimeform and endosulfan were used as experimental chemicals to demonstrate the presence of behaviour-modifying properties in conventional insecticides. Their modifying effect on the adult whitefly Bemisiu tubaci (Germ.) was observed and quantified under field conditions. Dosages of 500-2500 g/ha of chlordimeform and 960 g/ha of endosulfan caused irritation and mass emigration of the adults from the treated cotton foliage without producing detectable direct mortality. Laboratory studies using choice-chambers confirmed the repellent effect of these two compounds. The potential usefulness of behaviour-modifying properties in controlling a prolific and intractable pest such as the whitefly is discussed on the basis of a simplified model. An ideal type of behaviour modifier should be of simple chemistry, non-lethal to the pest, and environmentally safe. It should induce only irritation and continuous mobility of the pest in order to prevent it from feeding, mating and ovipositing. This is expected to reduce the population below the economic threshold without risking rapid selection for resistance which invariably results from the direct killing action of conventional insecticides. ABSTRACT.

Introduction

has been accused by Eveleens (1983) of destroying parasites and predators which he assumed to be essential in regulating the whitefly population. Clower and Watve (1973) and Watve and Clower (1976) reported that the effect of DDT and other broadspectrum insecticides on natural enemies was the cause of outbreaks of the banded-wing whitefly, Trialeurodes abutilonea (Haldeman) on cotton in Louisiana, USA. DDT has been suggested to stimulate egg-hatching and consequently causing population resurgence (Van der Laan, 1961). However, there has been some scepticism with regard to this suggested effect (El Bashir, 1974; K. G. Eveleens, personal communication). Recent laboratory investigations by Dittrich, Hassan and Ernst (1985) showed that DDT increased oviposition of B. tabaci by 30% and more importantly, produces a higher number of generations in a given period of time than the corresponding control without DDT. Selection of resistant individuals by conventional insecticides through decades of extensive spraying must have contributed to the exacerbation of the whitefly problem in the late 1970s. A 240-fold

Although the whitefly Bemisia tabaci(Genn.) has been recorded on cotton in the Sudan since the 1930s (Cowland, 1933), it remained an insignificant pest until the 1950s when an increasing research effort was made towards an understanding of its population dynamics and its control (e.g. Joyce, 1955; Joyce and Roberts, 1959; Van der Laan, 1961; Gameel, 1970, etc.). All these efforts reflected the growing importance of the whitefly as a pest. By the late 1970s it had become the ‘number one’ pest, replacing Heliothis armigera Hiibn. Whereas the latter could be controlled efficiently by aerial sprays of insecticides, the whitefly proved to be an intractable problem. Repeated sprays, eight times or more during the season, did not prevent the population from increasing steadily to as much as 10 times the economic threshold (Eveleens, 1983; S. Uk and R. Burden, unpublished work). Conditions leading to this major pest status of the whitefly may have been the combination of factors such as expansion and diversification of cropping, agronomic practices and the wide-scale use of conventional insecticides in conventional control efforts, first against Empoasca lybica de Berg. then against H. armigera, and recently against E. lybica, H. armigera and B. tabaci (to no avail against the latter). Extensive use of insecticides particularly of DDT, 0261-2194/86/05/0341-07

$03.00

0 1986 Butterworth

& Co (Publishers)

resistance

to dimethoate

was detected

among

field

populations of B. tabaci collected in the Sudan Gezira (Dittrich and Ernst, 1983) where dimethoate has been used continuously for more than 20 years. Resistance Ltd

342

Effect of insecticideson behaviour of Bemisia tabaci

to other insecticides was also present to a varying degree. B. tabaci is difficult to control by conventional spray methods. It reproduces rapidly in large numbers and lives on the lower surface of leaves in the middle of the canopy which protects it from chemical sprays. This paper discusses an alternative possibility to control this pest by exploiting the behavioural changes caused by established insecticides which seem to have a longer-lasting and stronger impact on the development of the population than their killing activity would lead one to expect. It is hoped that this new prospect will lead to more efficient use of chemicals at a frequency and dosage rate which are environmentally acceptable, economically attractive and thus appropriately adapted to the idea of integrated pest management.

Methods A sound basis for formulating an efficient control strategy requires the consideration of the pest behaviour and population dynamics in the field over an area which is commensurate with the practical scale. The behaviour-modifying effect of endosulfan was observed under large-scale spray practice which covered up to 10000 ha per day. Subsequent studies were undertaken starting with systematic macro-scale observations followed by small-plot experiments and laboratory tests under controlled conditions. The methods used are described below in a corresponding sequence. Endosulfan and chlordimeform, which have been known to affect the behaviour of lepidopterous larvae (Dittrich and LorZareviC, 1971), were chosen as experimental chemicals.

Large-scale field observations

The capability of insects to move long distances by taking advantage of the wind fields (Rainey, 1976; Joyce, 1983) necessitates sampling over as large an area as possible in order to monitor the movement of the population and its subsequent development. In the irrigated area of the Sudan, all fields are normally standardized to 1250 x280m (or 35ha) separated by water canals. Cotton occupies about 20% of the land and is interspaced by sorghum, groundnuts, vegetables and fallows. In 1980 two 35ha cotton fields, which were situated 1 km downwind of the cotton area to be sprayed with endosulfan, were selected as a monitoring site. The whitefly adults were counted (on 300 leaves from 60 randomly selected plants in each field) one hour before the start of the spray in the upwind area, then 6 and 24 hours afterwards. In 1981 two 35ha fields, located 5 km apart and in an area cultivated with 2000 ha of cotton, were chosen as observation sites in the axis of the North-South prevailing wind. Whitefly adults were regularly counted in these two fields. The wind direction and strength at the time of spraying and counting were estimated.

Small-plot field experiments

Chlordimeform and endosulfan were sprayed either in water mixture at the rate of 100 litres/ha using a pressurized knapsack sprayer, or in oil at ULV rates ranging from 1.2 to 12 litres/ha by means of a miniULVA spinning disc atomizer. Plot size was 20 x 20 m. All treatments were replicated three times. The effect was monitored by counting the number of adults before and each day following the application up to day 5. Counts were made on 30 plants selected at random from six rows and five plants per row in each plot. On each plant two top, one middle and two bottom leaves were gently turned over by twisting the petiole, to examine the number of whiteflies. Counts were made during the cool part of the early morning when the adults are less easily disturbed. Mortality, which would be evident by the dead adults on the upper surface of the leaves, was recorded qualitatively. Laboratory

tests

The adults of B. tubaci from a laboratory culture were placed in a choice-chamber which allowed them to choose freely between the treated and non-treated areas. The choice chamber was made from a plastic box 12 x 15 x 7cm. The inside of the box was lined with black paper and the box was covered with a piece of black cardboard. Two circular holes 3cm in diameter and 15 cm apart were punched out of the cover to allow small transparent medicine cups to be inserted. These cups served as the treatment areas. The bottom of each cup was lined with a 3 mm layer of agar to provide a moist substrate which is capable of keeping a leaf disc fresh for 5 days or longer (Hennequin and Auge, 1979; Dittrich and Ernst, 1983). Two cotton leafdiscs, one dipped in a sub-lethal concentration of either chlordimeform or endosulfan and the other untreated, were placed each on the agar surface with its physiological upper surface snug against the latter so that when the cups were fitted inverted on the cover of the choice-chamber, the leaf discs assumed their natural position to simulate the living environment of the whitefly. The choicechamber was made light-tight except the exits towards the plastic cups and leaf discs. The choice-chambers were placed in a plant-growth chamber which was evenly lit from above. Sixty adults were free to fly within the chamber towards, or away from, either of the two leaf discs. Counts of the adults resting on the leaf discs were made every 2 hours during the first day that they were introduced into the chamber, and every 12 hours subsequently for three days. Results Behaviour spraying

of the whitefly adults in the large-scale

Observations in 1980 showed that the number of adults in the unsprayed field downwind of the treated

S.UK TABLE 1. Mean adult whiteflies 5 SE in fields located areas treated with endosulfan (960glha) Date 10 Nov. 12 Nov.

Time 1980 1980

AND V. DITTRICH

1 km downwind

of

Adults/leaf 14 2 4

Morning: Afternoon:

1 h before spray 6 h after spray

28+-

24 h after

spray

25 * 1

3

N. wind

343

evidence that endosulfan sprays caused the whitefly adults to leave the treated field and to settle in the unsprayed area downwind. Close observations showed that the adults began to fly excitedly out of the cotton canopy about 30 minutes after it had been sprayed with endosulfan. From then on more and more adults were irritated and eventually a continuous mass exodus took place. The adults, being small and light, were carried away by the wind as soon as they were airborne. Adult behaviour in the small-plot experiments

N. wind 4 A+B

S. wind

IS~UTHI

var.

wind

S. wind

The effect of chlordimeform on the whitefly adults is presented in Figure 2. The reduction in adult numbers was the result of the latter being driven out of the area. No mortality within the plots was noticeable even when the infestation was very high. As the reduction in adult numbers was related to the dosage rates of chlordimeform, its behaviour-modifying influence would have acted through the vapour phase, the concentration of which would depend on the amount applied. Other evidence in support of the vapour phase hypothesis was that the adult reduction also occurred in untreated areas downwind of a plot treated with 2 500 g/ha of chlordimeform (Figure 3). Spray drift was not the cause, as the application was carefully done under cool and calm conditions. The adult reduction

FIGURE 1. Mean number of whitefly adults in regularly sprayed fields in the North-South line of the prevailing Inter-Tropical Front winds. J indicates sprays; A: deltamethrin; B: dimethoate; C: endosulfan.

area increased by 100% in 6 hours (Table 1). This increase by far exceeded the number that could be accounted for by new emergence from the pupae. The number remained the same after 24 hours. Counts which were made in four treated fields one day after spray showed that the number was reduced by 86 k 3% from an average of 23 adults to three per leaf. Mortality, if any, was negligible as there were no dead adults being fixed to leaves, as would be the case if an adulticide such as profenofos was used. When the latter was sprayed over fields of similar levels of infestation, the upper surface of leaves was coated white with dead adults yet the reduction was only 45 + 5% of the pre-spray number. In the 1981 study there was an alternative pattern of rise and fall in the adult numbers associated with the cycle of endosulfan sprays and wind direction in the two fields that were 5 km apart, chosen in the line of the North-South prevailing wind (Figure 1). The observations were made easy and reliable by the seasonal movements of the Inter-Tropical Front (a characteristic meteorological feature of Tropical Africa) over the Southern Gezira during October/ November which produces consistent wind strength of well-defined direction. On the two occasions when deltamethrin-dimethoate was sprayed, there were no definite patterns of adult increase in the downwind side although there was about 35% adult reduction after each spray. Thus the above results provided

405 30-s 3 s 20-

. P

10-a

: 2 d

l,..,,nn.,,lL

0

2

4

6

DAYS AFTER

FIGURE Vertical

0

10

12

14

2. Effect of various chlordimeform bars represent standard error.

loo/-

2500

wind

18

16

20

22

0

SPRAYING

dosages

on adult

whiteflies.

g ailha

_

z!50 El h 30 2

J+’t *

2.4

treated

FIGURE 3. wind.

49 * 4.0

?P

7.2

9.8

m

I

I

Effect

untreated of chlordimeform

rows

downwind

extended

into untreated

rows down-

344

Effect

of insecticideson behaviour of Bemisia tabaci

power decreased with increasing distance from the treated edge in accordance with the typical concentration gradient of the gas diffusion process. The effect of chlordimeform on the behaviour of lepidopterous larvae leading to loss of orientation and inhibition of feeding has been known for some time (Dittrich and LonEareviC, 1971; Doane and Dunbar, 1973). The behaviour effect on moths has also been reported (Salvisberg, Neumann and Voss, 1980; Shimizu and Fukami, 198 1). Endosulfan was tested at the rate of 960g/ha as recommended by the Sudan Pests and Diseases Committee. Its mode of action on the behaviour of adult B. tabaci is not yet understood. Visual observations showed that the adults became irritated 30 minutes after spraying. Increasing numbers flew out of the treated area and when they were airborne above the canopy they were blown downwind. The results from regular spraying during two seasons (September to November 1981 and 1982) showed that the irritation effect was of a density-dependent nature: as the density of adults on the cotton leaves increased, so did the level of the mass irritation and subsequent emigration from the treated plots (Figure 4). The reason for this density-dependence was not known. It could have been caused by a chain irritation due to physical crowding and/or the emission of an alarm pheromone by the adults which came into contact with endosulfan. No whitefly pheromone has been reported but an alarm pheromone of aphids, another type of small insect, is known (Griffiths and Pickett, 1980; Dawson et al., 1982). The reduction in adult numbers in relation to their

100 1

i

”

MEAN

10

5 ADULTS

FIGURE 4. Density-dependent endosulfan treatment one represent standard error.

15

PER LEAF

response of adult whiteflies to day after spraying. Vertical bars

”

”

ST

OCT

FIGURE 5. Density-related endosulfan effect.

field

treatment

sprays I””

30

10

20 NOV

reaction of adult whiteflies and rapid recovery from

to the

density on cotton leaves (Figure 4) followed a sigmoid curve which reached a plateau ofaround 90% when the density was 15 adults per leaf or higher. The plateau could have been due to continuous emergence from the large number of pupae which masked the real effect of the chemical. The rapid recovery of counts only one or two days after the dramatic reductions in adult numbers soon after endosulfan sprays was further evidence of this emergence from the pupae (Figure 5). Laboratory

01”“““““”

”

indicates

tests

Choice-chamber studies in the laboratory showed that in the control experiments when both leaf discs in each of the two cups were untreated, the adults were evenly distributed between them, i.e. each disc had an equal number of adults: 50 + 4% of the total introduced (Figure 6). Chlordimeform at 2-4pg/cm* of leaf caused lo-30% adults to stay away from the treated leaf discs (Figure 6). There was no mortality at any of the dosages used. Furthermore, there was no apparent difference between the two formulations of chlordimeform tested, namely the 20% flowable and the 50% emulsifiable concentrate. Endosulfan caused about 10% avoidance at 0 * 02pg/cm* after subtracting the effect of mortality (23 f 4%). At 0.1 pglcm*, there were no adults on the treated leaf discs. However, 50% of the introduced adults were dead underneath the treated cup whereas the remaining 50% were alive on the untreated discs. Endosulfan tested as a contact poison was very toxic to B. tabaci adults. Such toxicity

S.UKAND

was not observed in the field experiments. In their laboratory bioassays, Dittrich and Ernst (1983) reported an LD,, of l-6 ppm for endosulfan as compared with 825 ppm for chlordimeform (Dittrich et al., 1985). The above results proved that the repellent effect of cotton foliage treated with chlordimeform or endosulfan could be measured directly in laboratory experiments under controlled conditions. Discussion It is very difficult to control whitefly by spraying of conventional insecticides, because of its ability to reproduce rapidly in large numbers and its habit of living on the lower surface of leaves in the middle of the cotton canopy. The main object of spraying is to kill the pest either by direct contact as insecticide application or by secondary contact with contaminated plant surfaces. However, in the Sudan, frequently a rapid loss of activity is related to the evaporation of active ingredient at high temperature, and there is insufficient penetration of droplets into the canopy (Uk and Courshee, 1982). Furthermore, the development of the indigenous population with a great number of final stage nymphs ready to emerge at any time, masks any reduction effect in the population. As aerial spray application can act only on the adult stage, a simplified population model was devised to underline the problems encountered in controlling the whitefly.

0

untreated I

% live I 50I

I

untreated I I

I

100 O 1 days

8. CONTROL 100

;1 1 2

3

treated

untreated

CHLORMMEFORM 0 2pg cm-* a.i. 0 3pg II II I3 4 )Jg

II

FO 20 --5=--O-Op-

1 a*

CHLORDIMEFORM EC 50 0 3.6pg

cm-*a.i.

ENDOSULFAN 0 0.02 0 0.1

FIGURE 6. leaf discs.

Q Q

2

of adult

TABLE 2. Estimated population trends resulting from three different mortality rates if sprays were applied early in the season against the parent generation and at regular intervals against subsequent generations No. (d+ Approx. date Late Mid Early End Late

Aug. Sept. Oct. Oct. Nov.

Sprays + + -, +

Generation Parent Fl F2 F3 F4

TABLE 3. Estimated population mortality rates if sprays were subsequent generations

90%

95%

z(lcr+lQ)

2(10-+

14 104 747 5375

trends regularly

Late Mid Early End Late

Aug. Sept. Oct. Oct. Nov.

Population

Sprays

+ -* + -

of 98%

19)

2(10*+

7 26 93 336

resulting applied

No. (a”+ Approx. date

0) after mortality

19) 3 4 6 9

from three different against the F, and

9) after mortality

of

Generation

90%

95%

98%

Parent FI

2 144 1037 7465 53 748

2 144 518 1866 6719

2 144 207 299 430

F2 F3 F4

model

Extensive field observations in 1979 and 1980 showed that the duration of a generation (adult to adult peaks) averaged 24 days in September-October when there was regular large-scale spraying of insecticides. For practical purposes the average life of the female whitefly is thus taken to be 24 days. Based on earlier work by Gameel (1978) and others (Khalifa and El Khidir, 1964) each female is assumed to lay six eggs per day; three eggs would hatch into females and the other three into males. As the males will not contribute to the increase in future generations, they will not be included in the model calculation. On the basis of the above assumptions the population increase under different hypothetical spray strategies and effectiveness is illustrated in Tables 2 and 3. They show that mortality of up to 98% or higher of the parent and each subsequent generation is required from sprays in order to prevent the population from increasing to intolerable levels after 3-4 generations. Such mortality is practically impossible to achieve in the field by conventional insecticides. Individual tolerance, deposit variability and shielding of sprays by the canopy all contribute to the survival of the insect. Spraying to kill the adult whitefly is not, therefore, a promising approach. A possible alternative

EC 50

pg crri*a.i. pg I. 88

Presence

1

345

V. DITTRICH

0

Bemisia

tabaci

on treated

versus

untreated

The results presented above show that chlordimeform and endosulfan possess effective behaviour-modifying properties over the adults of B. tabaci. The repellent action observed on field-grown cotton could be reproduced in laboratory experiments for the first time. It may be an important facet of activity of other insecticides, which possibly has occurred more commonly

346

Effect

of

insecticides

on behaviour

than hitherto recorded. The effect of DDT on the behaviour of insects has been noted and studied since the 1940s. Kennedy (1947) investigated and discussed in detail previous reports on the excitation and repellency effect of DDT on mosquitoes. Repellency, irritation and forced mass emigration may be a most effective means of preventing the whitefly from settling to reproduce and establish the population within the cotton canopy. It is conceivable that constant irritation would prevent the adults from settling down to feed and oviposit, thereby imposing an increasing energy demand for sustained flight. Aflhcted insects are prone to succumb more readily to unfavourable environmental conditions such as heat and water stress which are prevailing in the Sudan. A control technique using this type of behaviour modification would probably require less chemical which, in turn, would lead to greater economy and environmental compatibility. A possible disadvantage may be that behaviour-modifying chemicals would increase pest mobility which could counteract their beneficial effect (Gibson et al., 1982) if the pest species is resilient to physiological and environmental stresses. In the case of the whitefly, the migrant females could each lay six eggs daily if they were allowed to settle in an untreated area for just one or two days before the latter received the chemical treatment. At present it is not known whether or not the affected adults would recover their normal behaviour, survive and reproduce normally or whether they would remain restless and fly off again after a short pause. It would be better still if behaviour modification could be achieved by compounds of simple chemical structure which are not lethal to the pest, so that selection of resistant individuals could be avoided. In such a case only unfavourable environmental and physiological conditions such as food deprivation, suppression of oviposition and exhaustion would be the limiting factors for the development of the pest population. In recent years great efforts have been made to put behaviour-modifying chemicals into practical use for the management of insect-pest populations (e.g. Wood, 19832 However the concept of 1980; Campion, behaviour modification to date is mainly related to studies of pheromones and their use to influence sexual or aggregation behaviour. Behaviour modification of a non-pheromonal nature, on the other hand, has attracted little attention. Pheromones of the whitefly are not yet known, but investigations with promising chemicals, as described here, may give an insight into, and provide solutions for, a more efficient and environmentally safe method of insect control. Conclusion The modification of the behaviour of B. tubaci by conventional insecticides is a possibility, as shown by the results of field and laboratory studies with chlordimeform and endosulfan. Large-scale population manipulation appears to be possible and may be

oj Bemisia tabaci

the most efficient and economic way to control a prolific and intractable pest such as the whitefly on cotton. Non-toxic behaviour modifiers which are environmentally safe would be the ultimate objective. Repressing a pest population to non-economically significant levels without directly killing the individuals would avoid, or at least delay, the selection process that will lead to eventual resistance. The ideal population modulators should impart damaging physiological effects to the pest through strong excitation coupled with restlessness which, in turn, would cause excessive use of energy resources resulting in loss of fertility or reduced mating and oviposition. Acknowledgements This work was supported by Ciba-Geigy Limited, Basle, Switzerland. The authors are grateful to CibaGeigy Services Limited in Sudan for logistic help and to the Sudan Gezira Board and the Sudan Agricultural Research Corporation for allowing the use of cotton fields. References CAMPION, D. G. (1983). Pheromones for the control of insect pests in Mediterranean countries. Crop Protection 2, 3-16. CLOWER, D. F. AND WATVE, C. M. (1973). The bandedwing whitefly as a pest of cotton. In: Proceedings, 1973 Beltwide Cotton January

Production

Research

Conference:

Phoenix,

Arizona,

1973, pp. 90-91. National Cotton Council ofAmerica. COWLAND, J. W. (1933). Gezira Entomological Section, GARS. Final report on experimental work, 1932/33. In: Sudan Government. Annual for the year

Report

of the Gezira

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fiir

allgemeine

und angewandte

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K. G. (1983). Cotton insect control in the Sudan Gezira: analysis of a crisis. Crop Protection 2, 273-287. GAMEEL, I. 0. (1970). The effect of whitefly on cotton. In: Cotton Growth in the Gezira Environment, pp. 265-280 (ed. by M. A. Siddig and L. C. Hughes). Sudan: Agricultural Research Corporation. GAMEEL, I. 0. (1978). The cotton whitefly Bemisia tabaci(Genn.) in the Sudan Gezira. In: Third Seminar on the Strategy for Cotton Pest Control in the Sudan, pp. 111-131. Basle: CibaGeigy Limited.

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JOYCE, R. J. V. AND ROBERTS, P. (1959). The determination ofthe size of plot suitable for cotton spraying experiments in the Sudan Gezira. Annals of Applied Biology 47, 287-305. KENNEDY, J. S. (1947). The excitant and repellent effects on mosquitoes of sub-lethal contacts with DDT. BuNetin ofEntomological Research 37, 593-607. KHALIFA, A. AND EL KHIDIR, E. (1964). Biology study on Trialeurodes lubia and Bemisia tabaci. Bulletin Soci&e’ entomologique d’Egypte 48, 115-129.

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R. C. (1976). Flight behaviour and features of the atmospheric environment. In: Insect Flight, pp. 75-l 12 (ed. by R. C. Rainey). Oxford: Blackwell Scientific Publications. SALVISBERG, W., NEUMANN, R. AND Voss, G. (1980). Chlordimeform: mode of toxic action in various developmental stages of Spodoptera littoralis. Journal of Economic Entomology 73, 193-196. SHIMIZU, T. AND FUKAMI, J. (1981). The effect of chlordimeform on the flight activity of the cabbage armyworm (Mamestra brassicae L.). International Pest Control 23, 166-175. UK, S. AND COURSHEE, R. C. (1982). Distribution and likely effectiveness of spray deposits within a cotton canopy from fine ultra low volume spray applied by aircraft. Pesticide Science 13, 529-536. VAN DER LAAN, P. A. (1961). Stimulating effect ofDDT treatment of cotton on whitefly (Bemisia tabaci Genn.) in the Sudan Gezira. Entomologia experimentalis et applicata 4,47-53. WATVE, C. M. AND CLOWER, D. F. (1976). Natural enemies of the bandedwing whitefly in Louisiana. Environmental Entomology 5, 1075-1078. WOOD, D. L. (1980). Use of behaviour-modifying chemicals in ecological considerations. integrated pest management: Ecological Bulletin 31, 41-56. RAINEY,

Accepted 1 January 1986