Sudanese cotton and the whitefly: a case study of the emergence of a new primary pest

CROP PROTECTION (1985) 4 (2), 161-176

S u d a n e s e c o t t o n and the whitefly: a case s t u d y o f the e m e r g e n c e o f a n e w p r i m a r y pest V. D I T T R I C H * ,

S. O. H A S S A N * * and G. H. E R N S T *

*Ciba-Geigy Ltd., CH 4002 Basel, Switzerland and **Ciba-Geigy Services Ltd, Wad Medani, Sudan Abstract.

In the late 1970s the whitefly Bemisia tabaci (Gennadius) became the primary cotton pest in the Sudan, superseding the American bollworm Heliothis armigera (Hiibner). D D T and a DDT/dimethoate combination were used to control the bollworm and, simultaneously, jassids and whiteflies. B. tabaci, a secondary pest at first, became resistant to dimethoate by frequent selections from 1964 onwards. At the same time, fertility stimulation occurred due to D D T residues on cotton plants. Finally, resistance reached a level so that the whitefly were not controlled by dimethoate, monocrotophos or other organophosphorus insecticides, and stimulation by D D T could exert its full effect. The consequence of this was a tremendous flare-up of the whitefly by 1980/81. This train of events was concluded from laboratory and field studies of the resistance patterns, as well as the acceleration effects from D D T residues on plants to the whitefly. A current hypothesis claiming that the problems arose from the elimination of beneficial insects through insecticide applications is reviewed in the light of experimental evidence and practical experience.

Introduction A major problem encountered in m o d e r n agriculture, particularly in monocultures of subtropical or tropical areas, is the emergence of new primary insect pests which were formerly o f secondary importance. As a rule this occurs as a consequence o f control efforts directed against a generally recognized primary target which appears on a seasonal basis and requires human interference to avoid intolerable damage to the crop. A secondary pest, by contrast, may not appear annually in significant numbers, or its control may be required only occasionally, when commercial damage is expected from an extremely heavy attack. T h e present work deals with the causes which converted Bemisia tabaci (Gennadius) in the Sudan from a secondary into the current primary cotton pest. M a n y reports have been written on the subject: some have been published in scientific journals and a sizable n u m b e r are registered as field documents of the 0261-2194/85/02/0161-16503-00 © 1985Butterworth& Co (Publishers)Ltd

162

Whitefly in Sudanese cotton

Agricultural Research Corporation (ARC) of the Sudan, or as Working Papers of the F A O / U N E P meetings of the experts on integrated control. Some important contributions may also be found in the proceedings of a number of symposia dealing with various aspects of the cotton culture in the Sudan. They have all contributed to the current discussion and will be taken up in this paper. The data presented below represent the results of experimental work carried out during three cotton seasons in Wad Medani, starting in 1981/82. Intensive laboratory work in Basel between seasons supplemented the field results. The emphasis was on the contribution of resistance (R, also used for resistant) to the whitefly (WF) problem, and on pest stimulation by D D T . Resistance in W F was often assumed to exist (Eveleens and Abdel Rahman, 1980; FAO, 1980), but there was no experimental proof until we started our work in the 1981/82 season. Stimulation of insect and mite pests resulting in flare-ups are well known in agricultural practice in the Sudan and elsewhere. The causes underlying this phenomenon have been the subject of much speculation in the past. One explanation maintains that the WF surge was based on the elimination of parasites and predators for which residues of environmentally stable insecticides are held responsible. Our data will serve to challenge this 'beneficial insect hypothesis' as promulgated by Eveleens (1983) and will offer a fresh view of the problem. Further, we hope to indicate new possibilities for better pest control in the Sudan on the basis of three years' research activities in Wad Medani, Sudan. Materials and m e t h o d s Measurement of W F fertility stimulation by D D T residues Two strains of B. tabaci were used: a sensitive strain, originally from the Sudan and cultured since 1978 in Switzerland, served as a reference for all R/S (LCs0R/LCsoS ( = R ratio)) figures in this work. The reaction to insecticides is sensitive and similar to that of another WF species, Trialeurodes abutilonea (Hald.) as reported by Watve, Clower and Graves (1977). This leads to the conclusion that the long culturing period in an insecticide-free environment has almost completely removed resistance genes from its genome. This strain has been reared, in our laboratories, only since 1981 although it was cultured in several other laboratories before this time. The R strain used in our experiments was collected from the Sudan only about 2 months before starting the experiments and some difficulties were encountered in producing the required number of teneral adults at the beginning of the work. A basic definition of adult reaction to D D T showed LCs0s to be 8"0 ppm (slope of regression line, b = 1.9) for S, and 77"5 (b = 1-9) for R. A recently hatched female and male were caged on a cotton leaf disc which was supported by a layer of agar to maintain leaf turgescence. The discs supporting WFs were dipped in a D D T emulsion at a concentration expected to be in a nontoxic range which, according to Luckey (1968), was suitable for eliciting hormoligosis. A comparable number of untreated pairs were maintained under the same conditions as the treated pairs in a climate chamber. The number of eggs was counted daily and the pairs were shifted to a freshly prepared plastic beaker with an agar-supported leaf disc. The cotton variety used was Dehapine 61 and the perspex containers had a volume of 25 ml with a base measurement of 25 mm

V. DITTRICH et al.

163

diameter. Two lateral windows closed by a piece of metal gauze prevented condensation inside the cage. Experimental insects were maintained at a temperature of 25-26°C and 80-90~o r.h. A photoperiod of 12 h light/dark was used during the experiments. The immature phase of the WFs under observation was also subjected to the influence of D D T : egg-waves (i.e. clumps of eggs of uniform age), obtained by releasing adults on to cotton plants in a flight cage, were dipped in D D T emulsions of 1, 5, and 10 ppm. These concentrations were also those on which adults were kept during their lifetime.

Measurement of toxic effects on adult WFs retrieved from Sudanese cotton fields Adult WFs were collected on the ARC experimental field in the early hours of the morning or at dusk. Insects dashing towards the light were caught in large glass jars and transferred to the laboratory in a cool-box to prevent damage. The testing technique corresponded to that described by Hennequin and Auge (1979) although modified according to our requirements. Discs of cotton leaves supported by a layer of agar about 1 mm thick were used as a substrate and were dipped in an ascending sequence of test concentrations of the respective toxicants. Small plastic Petri dishes were used as cages with mesh-covered holes on either side for ventilation, a rubber band fastening the two parts of the dish together. About 50 WFs were shaken into each dish and immobilized by CO2. After the cage had been closed the exact number contained was counted under a stereomicroscope. For each concentration tested two samples of about 50 adult WFs were treated, so that a dosage mortality line was computed on the basis of 2 x 5 0 x 5 = 5 0 0 individuals. Natural mortality never exceeded 7~o. The temperature was maintained at 25-30°C (r.h. about 30%).

Analysis of R mechanisms Carboxyesterase definition in vitro. Homogenates of single WFs of the S strain were used to demonstrate a putative R mechanism based on high esterase activity, by the hydrolysis of 0~-naphthylacetate and ~-naphthylbutyrate, and in addition that of 4-nitrophenylacetate. The homogenate was prepared by squashing a female W F in 1 #1 phosphate buffer pH 7-4. Esterases split the ester bond and free naphthol is formed which couples with Fast Blue B salt to form a blue stain. This is measured colorimetrically 10 min after the start of the reaction. In a similar test using 4-nitrophenylacetate as a substrate, 4-nitrophenol is liberated from its acetate by esteric hydrolysis and the resulting yellow stain is colorimetrically measured at 412 nm. Carboxyesterase activity measurements after previous incubation by OP inhibitors. Similar experiments were performed after inhibiting esterases by insecticides. I5o (50~/o inhibition) values were established for the S and R strains after 10 min pre-incubation with various concentrations of the respective inhibitors. A regression line was plotted and I5o values extrapolated. In vivo assay for esterases by spot-testing. T o substantiate the above laboratory investigation, extensive field assays were made based on the staining technique as

164

Whitefly in Sudanese cotton

described by Pasteur and Georghiou (1981) for mosquito larvae. Filter paper strips were impregnated with a solution of a-naphthylbutyrate and dried. Single WFs were squashed in 7/~1 bi-distilled H 2 0 on a Teflon ® plate and 5 ktl of the liquid taken up in a self-filling capillary. The contents of the capillary were completely discharged on predetermined spots on the filter paper strips. A vivid blue stain resulted if high esterase levels were present.

Cholinesterase sensitivity to inhibition by insecticide inhibitors in R and S strains The degree of inhibition of the target enzyme AChE was investigated using the method of Ellman, Courtney and Featherstone (1961) in which thiocholine is released from its acetate by AChE activity. It reacts with D T N B , forming a yellow stain, the intensity of which is measured in the colorimeter. As an enzyme source 80 female WFs were homogenized in 1 ml phosphate buffer pH 8.0 (2 mg/ml) which was diluted 1:3 to obtain the final enzyme concentration in the test.

Small-plot field experiments on insecticide performance against R whiteflies Plots of cotton, variety Acala, were laid out in randomized blocks with four replications. Each plot measured 15 × 25 m and contained 28 rows of 20 plants each. All plots were separated from neighbouring ones by bare strips of 2-4 m width. Preparations of insecticides were applied at a rate of 100 d/ha by a knapsack sprayer equipped with a boom and six nozzles. Applications were repeated whenever the population curves showed a strong upward trend. Six assistants and a supervisor counted the insects present early in the morning. In the centre of each plot five plants in a row were examined for the presence of adults on two top, one middle, and two bottom leaves. Every third day the counts were repeated. The curves in Figure 1 were plotted according to the method of cumulative insect days as suggested by Ruppel (1983). Insect days are defined as (x~-x2) (y2-yi/2) where YI and Y2 are insect numbers corresponding to two adjacent dates xI and x2. By adding consecutive days sequentially, cumulative insect days were obtained. In this work, cumulative insect days are expressed as the percentage difference to untreated. This technique allows comparative treatment of the data and permits an easy visual perception of the population movement.

Statistical treatment of the data Comparisons between WFs spending their adult life on DDT-treated or untreated cotton leaves were made by calculating means and standard deviations for female age, total eggs, and total eggs/female/day. The egg depositions per day per female were compared using a pooled t test. Toxicology tests were evaluated by probit analysis according to Finney (1971). A program was developed for the HP 41C computer which allowed computation of all important parameters of the regression analysis including confidence limits of LCs0 and slope as well as Z2 analysis for linearity under local conditions in the Sudan.

V. DITTRICH et al.

165

Results Stimulation of fertility by D D T residues

Table 1 shows the effect of D D T residues on reproduction and longevity of exposed WFs. In both a sensitive laboratory and a resistant field strain, the number of eggs/female/day were significantly different between treated and untreated groups (95~/o confidence interval (c.i.)). Variance in total numbers of eggs was high because of the high variation in individual lifetime, so that statistically significant differences could not be detected. However, even in the R strain at residue levels of 5 and 10 ppm there is a trend to higher egg-totals. Simultaneously, because of the effect of higher D D T levels, the average lifetime of the treated WFs is shorter than that o f the untreated. At the extreme level of 10 ppm the egg totals differ by 11~o, the treated egg-totals being the higher despite a 30~o shorter lifetin~e available for egg production. As the results from the intermediate D D T level conform to this trend, there seems little doubt that D D T residues on leaves directly stimulate WF fertility.

Resistance development in adults measured over 3 years

Resistance in Sudanese WFs is another key factor in explaining the rise of B. tabaci to the status of Principal pest of cotton. Tables 2 and 3 show that, against dimethoate and monocrotophos, R ratios of the order of 250 to 300X were the rule, reflecting selection intensity with both materials during the 1960s and 1970s. However, by 1981 neither D D T nor monocrotophos were being used any more, whereas dimethoate sprays were still in use. One consequence of this agricultural pattern was the reduction of R towards monocrotophos through successive seasons (Table 3), R ratios plateauing at 150X. Dimethoate values, however, were increasing steadily, a consequence of continued selection pressure. Carbofuran (as a representative of the carbamates) also showed increasing R, possibly directly related to dimethoate R, because neither carbofuran nor other carbamates were then in general use in the Sudan nor had they previously been used to any great extent. Other insecticides, such as endosulfan, D D T and cypermethrin, representing different chemical types of insecticides, are not subject to the highlevel OP-R mechanism evolved against dimethoate and monocrotophos. The action of neither profenofos nor chlorfenvinfos appears to be influenced by the prevailing OP mechanism: this is because the molecular structure of these compounds renders them difficult to metabolize. The highest R ratios were found for dimethoate and monocrotophos, insecticides of the OP type which were used for extended periods and in large quantities. A basic dimethoate R, resulting from treatments with the generally used insecticide DDT/dimethoate, must have developed as a consequence of a long sequence of selections with this combination which was introduced in 1964. Selections with monocrotophos started in 1972. R ratios in Table 3 indicate that there is a basic R mechanism common to both insecticides, but that monocrotophos selection also produced an R t y p e of its own, building on the basic dimethoate mechanism. This may be concluded from the reversion of the R ratios for monocrotophos to a value of 150X which o c c u r r e d after the use of monocrotophos had ceased, from 1981/82 onwards.

166

Whitefly in Sudanese cotton

TABLE 1. Bionomics of two strains (S +R) of Bemisia tabaci on cotton leaf discs with various levels of DDT residues Mean No. Period Concentration lifetime of of observed of DDT f e m a l e s Total eggs/ Total eggs/ Strain Treatment females (days) (ppm) (days) female female/day S S

Control DDT

25 25

38 38

0 1

R R R

Control DDT DDT

7 19 12

3442 4144 40

0 5 10

29.4 +8"8 309"0+115.2 28.6+7.0 344.8+119.8

10'6+2"2 12.0+2.4

37.6 +3.4 257.3 + 172.9 6-9 +4"7 30.7 +8"8 261.9 + 93"1 8"5 +2.1 26.7 +8"5 286.3 + 97.7 10.7+2.2

Identification of R mechanisms m adult WFs A convenient way of demonstrating the presence or absence of biochemical R mechanisms is to work on a comparative basis with R and S strains, as shown in Table 4a. Independent of the substrate used in the reaction with putative esterase preparations, values from the R strain indicated higher enzyme activity or amount, particularly with the substrate ~-naphthylbutyrate. The difference in activity observed between the butyl ester and other esters indicates that several enzymes are involved. Pre-incubation with insecticides shows that the butyrate-specific enzyme is more specifically inhibited by paraoxon and profenofos than is the acetate-specific enzyme; both are relatively insensitive to monocrotophos. This, also, indicates that at least two enzymes are present among the 'esterases' investigated (Table 4b). To determine how esterase activity was distributed in the field population in which the R measurements were made, hundreds of single WFs were tested with the spot-test as described under 'Analysis of R mechanisms'. Without exception the field insects reacted by producing a vivid blue stain indicating high esterase activity; however, differences in staining intensity were seen and evaluated. In stains from both males and females a 3 : 1 ratio of heavier to lighter staining was recorded. To interpret this as the expression of a single dominant gene would be premature although the idea is tempting. Further work is required to substantiate and confirm these speculations. Insensitivity of the target enzyme AChE is another important R mechanism which was tested by comparing S and R WFs (Table 5). The results show that Is0s of R and S AChE with carbofuran differ by a factor of 15, and with monocrotophos by a factor of two, although in the latter case a very shallow slope indicates a slow reaction with the inhibitor. Monocrot0phos was an important selectant for years and this may be the reason for this phenomenon. The figures indicate that AChE from the R strain differs from that in the S strain, with reduced sensitivity to inhibition. Both high levels of esterase activity and insensitive ACHE, therefore, form a combined R mechanism of great protecting power for their carrier.

6.7 12.2 4-9 1.3 12-3 20.0 11.8 2.7 0.2 2-4 20.5 1-6

Monocrotophos Dimethoate Profenofos Quinalphos Dicrotophos Chlorfenvinphos DDT Cypermethrin Decamethrin Carbofuran Aldicarb Endosulfan

5-7-7-9 9.8-15.0 4.4-5.4 1.1-1.4 9.6-15.7 16-4-24.3 9.4-14.7 2.1-3.4 0.18-0.27 2.1-2.9 17.9-23.6 1.3-2.0

c.i. 95% 3.2 2.8 4.3 7-0 2.0 3.0 2.2 1.6 1.7 3.6 4.8 3.5

b 1937 2877 45-0 119 895 -254 8.0 -460 -15.2

LCs0 1722-2179 2233-3707 36.1-56-1 94- 152 615-1302 -212-303 6.4-10.0 -401-525 -12.4-18.6

c.i. 95%

1981

3.3 3.6 2.6 2.1 2.0 -2.1 1.4 -3"0 -2.5

b 1068 3548 64-0 42 1199 112 98 29.1 1-8 -21.6 14.0

LCso 487-2339 3055-4120 50.8-80.6 37-48 986-1457 96-132 66-143 23.3-36.3 1.4-2.2 -18.6-25-1 11.0-17.8

c.i. 95% 1.6 3-0 2.0 3.9 2.3 2,6 2.0 1.6 1.6 -3.9 5.5

b

Centre group--field strain 1982

971 3804 64.3 46 888 111 166 40.8 2.7 722 48.3 12.9

LCs0

828-1140 3121-4638 52.5-78.7 40-54 767-1028 90-135 87-318 28.4-58"7 2.1-3.5 448-1164 44.0-53.0 9.1-18.4

c.i. 95%

1983

3.2 3-1 2.5 3-6 2.8 2-3 2.6 1.1 1-4 1.5 2.0 2.9

b

*Chemical names: monocrotophos: dimethyl (E)-l-methyl-2-(methylcarbamoyl)vinyl phosphate; dimethoate: O,O-dimethyl S-methylcarbamoylmethyl phosphorodithioate; profenofos: O-4-bromo-2-chlorophenyl O-ethyl S-propyl phosphorothioate; quinalphos: O, O-diethyl O-quinoxalin-2-yl phosphorothioate; dicrotophos: (E)-2-dimethylcarbamoyl-l-methyh,inyl dimethyt phosphate; chlorfenvinphos: 2-chloro-l-(2, 4-dichlorophenyl)vinyl diethyl phosphate; DDT: 1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane; cypermethrin: (RS)-~-cyano-3-phenoxybenzyl (1 RS, 3RS; 1RS, 3SR)-3-(2,2-dichlorovinyl)-2,2-dimethylcyclopropanecarboxylate; decamethrin (deltamethrin): :(S)-~-cyano-3-phenoxybenzyl (IR, 3R)-3-(2,2-dibromovinyl)-2,2-dimethylcyclopropanecarboxylate, carbofuran: 2,3-dihydro-2,2-dimethylbenzofuran-7-yl methylcarbamate; aldicarb: 2-methyl-2-(methylthio)propionaldehyde O-methylcarbamoyloxime; endosulfan: C,C~-(1,4,5,6,7,7-hexachloro-8,9,10-trinorborn-5-en-2,3-ylene)(dimethyl sulphite).

LCso

Reference strain

Toxicology data for adult Bemisia tabaci tested over three cotton seasons in Wad Medani, Sudan

Insecticide*

T A B L E 2.

~q ~q

168

TABLE 3.

Whitefly in Sudanese cotton

R ratios (LCso R strain/LCs0 S strain) for adult Bemisia tabaci tested over three cotton seasons in Wad Medani, Sudan

Insecticides

1981

Monocrotophos Dimethoate Profenofos Quinalphos Dicrotophos Chlorfenvinfos DDT Cypermethrin Decamethrin Carbofuran Aldicarb Endosulfan

290 236 9 92 73 -22 3 -190 -10

TABLE 4.

Seasons 1982

1983

160 290 13 32 97 6 8 10 9 -1 9

150 311 13 36 72 6 14 14 13 300 2 8

Carboxyesterase activity in adult Bemisia tabaci

(a)without previous inhibition by insecticides* Activity Substrate 0~-naphthylacetate# 0¢-naphthylbutyratet 4-nitro-phenylacetate~

S strain

R strain

R/S

182 roOD 94 roOD 20 mOD/min

625 mOD 1860 mOD 57 mOD/min

3.4 20 2"9

(b) Is0 values of S in ppm after 10 min pre-incubation with various insecticides Substrates Inhibitor

Paraoxon Monocrotophos Profenofos

~-naphthylacetate

~-naphthylbutyrate

0-067 >> 3-3 1 *Homogenates: 1 female/ml in phosphate buffer pH 7.4 ~'Measured as naphthol with Fast Blue B salt after 10 rain :~Measured at 412 nm

0.002 8-3 0.012

169

V. DITTRICH et al. TABLE 5. Cholinesterase inhibition in adult Bemisia tabaci* Pre-incubation time (min)

Iso (ppm)

b?

Carbofuran Monocrotophos

1 10

0-06~).09 17

1.4 1.3

Carbofuran Monocrotophos

1 10

1 35

0'7 0"2

Strain

Inhibitor

S R

*Homogenate:80 individuals = 2 mg/ml; Control activity:15-25 mOD/min tSlope of regressionline

Demonstration of R in WFs infield experiments

Figure 1 demonstrates the effect of R towards different types of insecticides used at recommended rates in commercial formulations: aldicarb (Temik ®) at 2750 g a.i./ha, cypermethrin (Polytrin ®) at 480 g a.i./ha, and monocrotophos (Nuvacron ®) at 2800 g a.i./ha. The total amounts were applied in four sprays or, in the case of aldicarb, in one root-zone application of the granular formulation. T h e respective R ratios from Table 3 are aldicarb 2, cypermethrin 14, and monocrotophos 150. Figure 1 shows the effect of sequential treatment of the WF population by these insecticides. In the graph the untreated control is represented by the 0 line (0°/0 reduction). The trend of the curves agrees with the R ratios for the respective insecticides. Monocrotophos, with the highest R ratio, shows a negative percentage population reduction curve, i.e. an increase over untreated. Cypermethrin, with an R ratio of 14, achieves a control effect of about 40% throughout the test period, and the corresponding value of aldicarb, R ratio 2, after granular application to the plants' roots, produced the highest control effect of about 80~o. The toxicological R data correlate with the results of the field experiments, even though there were differences between the mode of action, rates used, and stage-specific toxicity of the three insecticides. Discussion Stimulation of insect or mite pests on various crops by D D T and other insecticides is a phenomenon which has been recognized since the early days of their use in horticulture. Since Hueck, Kuenen, DenBoer and Jaeger-Draafsel (1952) investigated the effect on the European red mite on apple, many studies have been carried out to elucidate its mechanism in the field as well as in the laboratory (Van de Vrie, McMurtry and Huffacker, 1972; Dittrich, Streibert and Bathe, 1974). Numerous reports from the Sudan testify to flare-ups of Bemisia tabaci as a consequence of D D T treatments to control Heliothis armigera (Hiibner), or, from 1964, following DDT/dimethoate sprays to control the pest complex of bollworm, WF and jassid. Publications by Joyce (1955), Joyce and Roberts (1959), Van der Laan (1961), and others have indicated the interdependence of D D T application and subsequent WF problems, and a recent publication by Satpute and Subramaniam (1983) has described the same problems

~

-40

-20

20

4O

60

80

I00

0

II

III I

t IIII

20

I

q

I ...... Days of treament

30

I 40

FIGURE

50

I

IIII

-- --Lk

-~.A-°-----A °-~.o./~ H ii

IIIIIIIIIIIIIIIIIIIIIIIIIII

A--

-----*0--

l. Cumulative insect days under treatment with three insecticides. Counting dates marked by code symbols, applications by arrows. O O Aldicarb 1 x2.75 kg/ha: A . . . . A cypermethrin 4 x 120 g/ha; 1-1--.--El monocrotophos 4 ×700 g/ha.

I0

IIII

0

o/

o/-

c~/0

IIII1

L~

60

e~

g~

2'

V. DITTRICH et al.

171

after phosalone ULV application in India. El Bashir (1974) could not confirm Van der Laan's hypothesis of higher hatching rates of eggs after D D T and also failed to assay a higher egg-laying rate of females on D D T at concentrations one hundred times higher than those described in our experiments. Clearly, toxic conditions prevailed in this range and hormoligosis could not be observed, because the stressor capacity of D D T and other insecticides is exerted only if they are present in non-toxic amounts (Luckey, 1968). Many other laboratory studies on various insect groups have now confirmed the early demonstration of stimulation of the fertility of mites by contact with D D T and carbaryl residues. Kirillowa (1973) observed increased egg-laying in Heliothis armigera after DDT. Various insecticides such as carbaryl, methyl-parathion, chlorpyrifos, phospholan, and mephospholan applied to different larval stages of Spodoptera littoralis (Boisduval) caused toxic effects at high dosages, but accelerated egg production by the moth after larval treatment with low dosages of insecticide (Esaac, E1 Gogary, AbdelFatah and Maher Ali, 1972; Mansour, 1978). In Coleoptera, D D T caused increased egg production upon injection into Leptinotarsa decemlineata (Say) (AbdaUah, 1968), and in Diabrotica virgifera (le Conte), carbaryl and carbofuran significantly increased fertility and longevity at low dosages, as shown by Ball and Su (1979). In Homoptera~ Chelliah and Heinrichs (1980) found stimulation of fertility of the delphacid Nilaparvata lugens (St~l) after methyl-parathion, diazinon and decamethrin. The phenomenon of acceleration is, therefore, well documented. We have used the term 'acceleration' for all stimulatory effects exerted on target or non-target species. We understand the term 'resurgence' as applying to the special situation when initial control of a target pest was achieved, with a subsequent flare-up. However, such an effect is also observed in response to 'non-toxic' materials, for example D D T and carbaryl in the case of mites. In this instance 'acceleration' is the better term. It also permits the use of the correlated term 'deceleration' for which there is a definite need in our discussions. Our results as shown in Table 1 are in agreement with the above-mentioned examples of acceleration through increased fertility. A higher number of eggs produced, even if toxic effects start to be seen at increasing D D T dosages, is strong evidence that hormoligosis is o n e causative factor of the WF surge on Sudanese cotton. The stimulation is direct and not delayed, and it corresponds to that observed in Tetranychus urticae (Koch) under similar conditions (Dittrich et al., 1974). Since D D T or mixtures with D D T were used for the three earliest seasonal sprays to control H. armigera (Hakim and Nasr E1 Din, 1978) a stimulus from D D T residues of variable intensity due to gradients orig:~nating from differences of spray exposure and residue degradation over time is provided during the important phase of WF build-up. Thus, there is hardly any doubt that WF populations have been accelerated during early season treatments. Cessation of D D T application by order of the Ministry of Agriculture in the 1981/82 season and the following decline of WF counts seem to corroborate these conclusions (Table 6). At the same time the incidence of the bollworm H. armigera was reduced: the idea persists that Heliothis problems, too, may have been caused by resurgence after D D T . Certainly, the results with Lepidoptera discussed above, in particular those of fertility stimulation in H. armigera as reported by Kirillowa (1973), lend support to this speculation. At any rate, one of the basic factors of the WF problem in the Sudan is hormoligosis with increased egg-laying attributable to the ever-present D D T residues on the cotton crop. The total amount of D D T

172

Whitefly in Sudanese cotton

applied in 1974/75, according to a statistic of E1 Bashir, El Tigani and E I T o m (1978) was 1428 metric tons (t) ofa.i, or 60% of the insecticide total. This is by far the largest amount of any single chemical used for pest control on Sudanese cotton and it maintained this position until its withdrawal in 1981/82 (Eveleens, 1983). The second major factor causing B. tabaci to adopt the role of a primary pest is R against ~the main OP insecticides dimethoate and monocrotophos. Resistance was often suspected, as indicated in the Introduction. However, the first published evidence--R figures for the 1981/82 season by Dittrich and Ernst (1983) appeared only recently. Tables 2 and 3 of the present paper extend this evidence and also indicate the dynamics of R. This is particularly interesting after the TABLE 6.

Counts of adult Bemisia tabaci on cotton in the Sudan Gezira during the last years. Average adults/100 leaves. Source Sudan Gezira Board

Season

September

October

November

December

1979~80 1980'81 1981'82 1982'83 1983'84

43 103 45 8 41

186 228 132 42 133

250 985 399 174 259

650 1565 686 338 313

cessation of monocrotophos use in 1981/82. LCs0s for monocrotophos fell to half the 1981 level, whereas those for dimethoate rose continually, because of continued use of this selectant in combination with other insecticides such as decamethrin. R ratios for monocrotophos levelled off at 150X: a basic OP-R selected for, and maintained by, dimethoate can therefore be postulated. As dimethoate R provides cross-resistance for many other OP-insecticides and has the longest tradition of selecting WFs in the Sudan, this is a fair assumption. Other OPs, such as dicrotophos, chlorfenvinphos, and quinalphos, are moderately or slightly affected by cross-resistance. Profenofos is an insecticide which is hardly affected. All other insecticides (endosulfan, D D T and pyrethroids) are not subject to the existing R mechanism; carbofuran, however, seems to be directly affected by it, as its R ratio increased parallel to that of dimethoate. Regular carbamates lacking the oxime moiety are not used currently for insect control and have been used only sparingly in the past. Supporting evidence that dimethoate provides the strongest selection pressure among the OPs comes from the application statistics. In the 1974/75 season the amount of this insecticide used in the Sudan was 876 t, i.e. 37~/o of the total, whereas the figure for monocrotophos was 77 t or 3~o (El Bashir et al., 1975). No complete statistics are available for the ensuing period, but it may be assumed that the percentage of monocrotophos rose from 30/o in 1974/75 at an increased rate. Nevertheless, dimethoate by frequency of selection and total amount applied was, and remains, b y far the strongest selectant for R..To some extent this is reflected by work with the jassid Empoasca lybica (De Berg.) which we undertook during the 1983/84 season. The LCs0 for dimethoate did not conform to the cluster o f results obtained from other insecticides. In fact, depending on the respective baselines; it exceeded them by about four- to eight-fold. These findings emphasize the

V. DITTRICH et al.

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dangers implicit in the continuing use of a strong selectant for R such as dimethoate. The nature of R in adult WFs and its occurrence throughout the field population in Wad Medani is demonstrated in Tables 4 and 5 and the unpublished data of the spot test. These show that high esterase activity and an insensitive cholinesterase form a compound R mechanism which is a potent protectant for its carrier. Increased mixed function oxidase (MFO) activity may also be present, but our results (which are not presented here) are ambiguous because the M F O inhibitor used to analyse the presence of M F O s had considerable toxicity of its own on WFs. The gene for high esterase activity seems to be distributed throughout the W F population, as demonstrated by the spot test with single WFs collected in great numbers in the field. Laboratory work on I{, close to the field as it may be, must always be related to field results to demonstrate its validity. The data of Figure I must be interpreted with this in mind. They show the result of sequential treatments of cotton in a randomized block experiment with counts performed every third day. Despite unavoidable differences in dosages applied, attributable to the nature of the insecticides, the curves reflect the degree of R against the respective chemicals: the lowest degree of control was obtained for monocrotophos, and the best control effect resulted from aldicarb treatment via the soil. Thus, field results echo toxicology experiments; this finding is reinforced by the intermediate curve of cypermethrin. On the basis of the findings regarding D D T acceleration and OP resistance, we can now suggest with confidence a hypothesis of the causes which led to the W F dilemma in the Sudan. The key to this process is the control of the long-term primary pest, H. armigera. We have shown that D D T provided a stimulus for the secondary pest B. tabaci which was also present, and possibly for the target itself, the bollworm. Through the years from 1964 onwards, selection pressure was exerted by dimethoate at least during the first three sprays of the season, often during six sprays (Hakim and Nasr E1 Din, 1978). Initially, the purpose of keeping jassids, W F and aphids at_an acceptable level by adding dimethoate to the basic D D T spray was successful. In the words of Eveleens and Abdel Rahman (1980) 'the direct outbreak-inducing effect of D D T . . . is masked b y the addition of compounds like dimethoate and methyl-parathion which suppress whitefly'. The critical stage was reached when the WF escaped from control by dimethoate, because of R development; this phase was reached i n t h e second half of the 1970s. Then WFs could react fully to the acceleration effect of the ever-present D D T , without being checked any more by an effective toxicant. This, to an increasing extent, was also true for monocrotoph0s and other OPs which, to a varying degree, were subject to cross-R from the dimethoate mechanism. Selections with monocrotophos, occurring at increasing frequency from 1975 on, produced a specific R type which was built on that of dimethoate R to result in a situation such as that described for the 1981/82 season in Table 3. This explanation of the train of events is in contrast to a different school of thought which postulates the elimination of parasites and predators as the main factor influencing W F dynamics. Eveleens (1983), Eveleens and Abdel Rahman (1980), and Bindra and Abdel Rahman (1983), were critical of chemical plant protection and strong supporters of the 'beneficials' hypothesis. Even though we share many of their views, there are some points of their argument which require

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critical discussion. On the basis of our own results and those of other workers, there are serious reservations with regard to the importance of biological control for the regulation of the W F dynamics. This is the pivot of their interpretation of the W F problem. In 1978 Eveleens, El Tigani and E1 Amin expressed their ideas with some restraint and as a result of a process of elimination; in 1980 Eveleens and Abdel Rahman presented it with more conviction but still with little factual material to support their conclusions: 'the rapid worsening of the W F situation in late season in conjunction with the depletion of parasities and predators lend support to the idea that killing of natural enemies of whitefly by insecticides is a major factor involved in this development'. As we have seen, other explanations are possible. Published data on the degree of WF parasitization showed great variation, ranging from 44~/o in December (Gamed, 1969) to 90-100°/o (Joyce, 1955). Insecticide sprays may reduce the degree of parasitization, as was stated for D D T (Gameel, 1969), but on the other hand there is evidence for the presence and, indeed, great resilience of parasites and predators to chemical treatment (Bindra and Abdel Rahman, 1983). It is clear from our own work that the local distribution of parasitized pupae may vary from 0~/o to as much as 82~o on large areas checked with a distance of only 3 km between fields. Patchy occurrence and a delayed density pattern of parasites following the host dynamics (Cowland, 1933, 1934; Bedford, 1935; Gameel, 1969) cannot be expected to relieve W F pressure efficiently when it really counts, namely at the beginning of the season and before the damage is done. Later, scale densities of about 150/cm2 may be reached (Tothill, 1948). In these circumstances at any degree of parasitization the crop will suffer, in particular with regard to honeydew contamination. On the basis of these facts we maintain that there is not enough evidence to support the 'beneficials' hypothesis as promulgated by Eveleens (1983) and others. We do not deny a supporting role of beneficial insects in exerting some constraint on W F development towards the end of the season. Nevertheless, we maintain that the key to the W F dilemma was D D T as an accelerator of fertility and dimethoate and monocrotophos as selectants for resistance. Compared with this, the partial elimination of beneficials was an event of minor importance. Other contributing factors could not be considered within the framework of this research: for example, the influence of plant variety and plant physiology with factors such as fertilization and irrigation being important variables. The same is true for socio-economic factors which, during the last few years, have considerably influenced Sudanese agriculture. One of the most important necessary steps was taken in 1981--namely, the withdrawal of D D T - - a n d this has probably helped to reduce W F pressure during the last three seasons. Insecticides which accelerate whitefly population growth should be avoided and 'decelerators' favoured. The elimination of dimethoate from the range of currently used insecticides is long overdue in view of its ineffectiveness against resistant WFs and its role as the most important R selectant for OP R. Suitable insecticide mixtures to fill the resulting gap have been developed and these offer more efficient W F control due to a potentiating effect between their components. A more distant goal is the development of insect population 'modulators' rather than the traditional insecticides. These will be based on a mode of action rather different from straightforward toxicity. Great efforts are required, and patience must be exerted, to move towards this goal.

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Acknowledgement M u c h o f o u r field work was carried out in the experimental fields o f the A R C , W a d Medani. T h e c o - o p e r a t i o n and kind s u p p o r t o f D r M . El T i g a n i are greatly appreciated. T h e a u t h o r s are further i n d e b t e d to M r C. K r a m e r for carrying out the in vitro e n z y m e assays o f this work.

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