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Selectivity evaluation of insecticides used to control

tomato pests to Trichogramma pretiosum

Alexandre Pinho MOURA*, Geraldo Andrade CARVALHO, Adriano

Elias PEREIRA and Luiz Carlos Dias ROCHADepartment of Entomology, Federal University of Lavras, Campus da UFLA, Lavras,

Minas Gerais, 37200-000, Brazil

*Author for correspondence (e-mail: [email protected])

Received 12 September 2005; accepted in revised form 6 January 2006

Abstract. The effects of the insecticides abamectin, acetamiprid, cartap and chlor-

pyrifos on larvae, pupae (within the host egg) and adults of the egg parasitoid

Trichogramma pretiosum Riley (Hym.: Trichogrammatidae) were evaluated under

laboratory conditions, using three standard tests described by IOBC. When sprayed

on the immature stages of this parasitoid, cartap and chlorpyrifos proved to be the

most harmful insecticides, affecting both the emergence success and parasitism

capacity of this parasitoid, whereas abamectin and acetamiprid were selective.Abamectin was harmful to adults (residue test on glass plates), slightly harmful to

larvae, and moderately harmful to pupae (sprayed on the immature stages within

host eggs Anagasta kuehniella (Zeller)); acetamiprid was moderately harmful to

adults, harmless to larvae, and slightly harmful to pupae; cartap was harmful to

adults, moderately harmful to larvae and harmful to pupae; chlorpyrifos to adults,

harmless to larvae and harmful to pupae.

Key words: biological control, egg parasitoid, Hymenoptera, pesticides, natural ene-

mies, side effects, Trichogrammatidae

Abbreviation: IOBC International Organization for Biological Control

Introduction

Egg parasitoids are known to be very effective against a number of

crop pests. Parasitoids belonging to the genus Trichogramma have

worldwide distribution and play an important role as natural enemies

of lepidopterous pests on a wide range of agricultural crops (Hassanand Abdelgader, 2001). During the last decades, Trichogramma wasps

have been used as biological control agents for pest suppression in

several countries (Abdelgader and Hassan, 2002). The use of reared

BioControl (2006) 51:769778 IOBC 2006

DOI 10.1007/s10526-006-0001-x


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Trichogramma spp. in biological control has gained widespread inter-

est in many countries (Hassan et al., 1998).

Due to the importance of Trichogramma spp. as natural enemies ofseveral pests, the study of pesticides selectivity to them is of major

importance for their role as biological control agents.

The species Trichogramma pretiosum Riley (Hym.: Trichogrammat-

idae) is an important natural enemy and the most promising biologi-

cal agent used to control Tuta absoluta (Meyrick) (Lepidoptera:

Gelechiidae) in tomato crops in several countries in South America

(Consoli et al., 1998). In northeastern Brazil, this parasitoid has been

successfully used to control the tomato moth T. absoluta in field and

greenhouse conditions, in which parasitism rates of 42 and 68% wereobserved, respectively (Haji, 1997). As the use of insecticides is a com-

mon practice among tomato producers, the use of selective pesticides

is an important strategy for the maintenance of Trichogramma popu-

lation within the crops.

However, there are few published studies about the effects of the

pesticides used to control tomato pests on this parasitoid. Therefore,

the effects of some pesticides used in this crop on different stages of

T. pretiosum, using three types of standard tests recommended by the

International Organization for Biological and Integrated Control of

Noxious Animals and Plants (IOBC), West Palaeartic Regional Sec-

tion (WPRS), were evaluated.

Material and methods

Parasitoid rearing

Stock populations of T. pretiosum were maintained on eggs of the

factitious host Anagasta kuehniella (Zeller) (Lep.: Pyralidae) under

controlled conditions at 241 C, RH of 7010% with 12 h of pho-

tophase. The alternative host was reared on a diet based on whole

wheat flour (97%) and brewers yeast (3%). The host eggs were glued

on blue paper cards impregnated with Arabic gum diluted in 50% of

water and UV-killed before being offered to parasitism. After the par-

asitism period (24 h), parasitized eggs were transferred to new con-

tainers (glass tubes of dimension 8.5 cm height 2.5 cm diameter)and kept in incubators until adult emergence, at the same controlled

conditions previously described.

ALEXANDRE PINHO MOURA ET AL.770


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Pesticides

Commercial formulations of the pesticides were diluted in distilledwater at concentrations recommended for tomato crops, which were:

acetamiprid (Mospilan 200 PS 0.05 g a.i./l), cartap (Thiobel 500 PS

1.25 g a.i./l), abamectin (Vertimec 18 CE 0.018 g a.i./l) and chlor-

pyrifos (Vexter 480 CE 2.40 g a.i./l). Distilled water was used as

control.

Initial toxicity test

This bioassay was carried out by exposing adults of T. pretiosum toresidues of the pesticides applied on glass plates. The test followed

the methodology described by Hassan et al. (2000) and Zhang and

Hassan (2000). The exposure cage consisted of an aluminum frame

(1313 cm, with walls 1.5 cm high and 1 cm wide) with holes forventilation. The upper and lower surfaces were covered by foam to

provide pads for two glass plates (2 mm, 1313 cm). The glassplates were treated with the evaluated pesticides using a Potters

tower, ensuring a deposit of 1.681.95 mg cm)2 on the glass plates,

which were subsequently maintained at environment conditions to

dry.

The glass plates were then fitted onto the square aluminum frame

forming the floor and ceiling of the exposure cage. Three sides of the

aluminum frame had six ventilation holes (1 cm diameter), with its in-

ward surface coated with black, tightly stretched, porous material to

cover the ventilation holes and prevent parasitoids from escape. The

fourth side of the aluminum frame had two different holes. The smal-

ler one was used to introduce the parasitoids. The second bigger holewas used to introduce the UV-killed eggs of A. kuehniella for parasit-

ism and food (honey) for the parasitoids, with the host eggs being ad-

ded at 2, 3 and 5 days after the beginning of the test.

In order to increase the contact of the parasitoids with the treated

surface, the exterior edges of the glass plates were covered with black

paper cards. A central square (55 cm) was cut out from the blackpaper cards, thus establishing a contact area of the insects to the

plates containing residues of pesticides within the illuminated area.

The cage was held together with two strong bands. The cages wereconnected to a vacuum pump via a tube system to prevent possible

accumulation of pesticide vapors. The pump was adjusted so that

the entire air in the cages was removed by suction at intervals of

12 min.

SELECTIVITY EVALUATION OF INSECTICIDES 771


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Emergence tubes (Eppendorf type) containing parasitized eggs of

A. kuehniella glued with diluted Arabic gum on 0.5 cm2 (250

eggs) of a 32 cm blue paper cards were used to introduce thestarting population of parasitoids to the interior of the cages. Two

days before emergence, the black eggs containing pupae of the par-

asitoids were transferred to the tubes. A little drop of honey was

directly applied on the inner surface of each tube as food source

for the parasitoid wasps. The smaller end of the tubes were re-

moved and the tubes connected to the cages. Each tube, before

being connected to the cages, was covered with a dark material to

induce the entrance of the parasitoids to the interior of the cages.

The emerged adults were left in the emergence tube until becoming24-h old.

The effects of tested pesticides were determined through assessment

of the parasitism capacity. Six replicates were used for each treat-

ment, each replicate being composed by one exposure cage containing

about 250 eggs of A. kuehniella. In this test, the number of emerged

adults ranges from 105 to 138 in each replicate.

Larvae and pupae toxicity tests

These were performed following the method described by Hassan

and Abdelgader (2001). One-day old A. kuehniella eggs previously

UV-killed were glued on strips of blue paper cards with diluted Ara-

bic gum on 0.5 cm2 (250 eggs) and parasitized by T. pretiosum for

24 h. The parasitized eggs were left for 2 and 7 days (larvae and pu-

pae tests, respectively) at 241 C, RH of 7010% with 12 h of

photophase. These paper cards with parasitized eggs were then trea-

ted with the pesticide or distilled water (control) by using a Potterstower. Eight replicates were used to assess the side effects of the tes-

ted pesticides in the larvae test and seven replicates in the pupae

test. The adult emergence and parasitism capacity of T. pretiosum

were evaluated. For these bioassays, the same exposure cage and

emergence tubes used in the initial toxicity test, but using untreated

plates, were utilized.

The pesticides were classified as suggested by the IOBC/WPRS

(Sterk et al., 1999): class 1 (harmless) < 30% of reduction either in

the parasitism capacity or in the emergence, class 2 (slightly harm-

ful)=3079% of reduction, class 3 (moderately harmful)=8099% of

reduction and class 4 (harmful) > 99% of reduction. For this test, the

number of emerged adults ranged from 81 to 142.



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Statistical analysis

The obtained data were submitted to analysis of variance (ANOVA)and means were compared by a cluster analysis method for grouping

means using the ScottKnott test (p < 0:05) (Scott and Knott, 1974)when the F-test was significant. Analyses were performed using the

SAS program (SAS Institute, 2001). Data related to parasitism rate of

adults (in the adult, larvae and pupae tests) were transformed toffiffiffiffiffiffiffiffiffiffiffiffiffiffiffix 0:5

p, whereas those related to the percentage of emerged adults

(in the larvae and pupae tests) were transformed to arc sinffiffiffiffiffiffiffiffiffiffiffiffiffix=100

p.

Results

The parasitism capacity of T. pretiosum females exposed to treated

surfaces was affected by all evaluated pesticides. Acetamiprid reduced

the parasitism in 98.3%, and was classified as moderately harmful

(class 3=8099% effect), whereas abamectin, cartap and chlorpyrifos

were harmful (class 4 > 99% effect) (Table 1). For the pesticides car-

tap and chlorpyrifos, high mortality of adults was verified in the inte-

rior of the emergence tubes.

Table 1 shows also the effects of the evaluated pesticides on larvaeof T. pretiosum within eggs of A. kuehniella. When eggs of the alter-

native host containing the larval stage of T. pretiosum were treated,

only cartap significantly reduced the emergence of this parasitoid,

allowing emergence of 45.7% and being classified as slightly harmful

(class 2=3079% effect). For the compounds abamectin, acetamiprid

and chlorpyrifos, the emerging adults ranged from 63.2 to 70.8%, not

differing significantly from the control. Thus, abamectin, acetamiprid

and chlorpyrifos were harmless to this parasitoid, causing reductions

lower than 13% in its emergence.

The parasitism capacity of T. pretiosum females from treated

larvae within eggs of A. kuehniella was affected by abamectin and car-

tap, differing significantly from other treatments. The number of eggs

parasitized per female from eggs treated with acetamiprid and chlor-

pyrifos was 36.3 and 34.6, respectively. Acetamiprid and chlorpyrifos

were classified as harmless, whereas abamectin and cartap were slight-

ly harmful and moderately harmful, respectively (Table 1).

The pesticides which were harmful and moderately harmful toadults in the surface test were further tested at the pupal stage of

T. pretiosum (the less susceptible life stage) within the host eggs

(Table 1). The results revealed that cartap and chlorpyrifos were

harmful to T. pretiosum when applied on host eggs containing the



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pupal stage of this parasitoid, reducing the emergence of individuals

from host eggs treated with these pesticides. In this bioassay, abamec-

tin and acetamiprid were harmless, causing reductions lower than

Table 1. Effects of some insecticides on T. pretiosum by different exposure forms.

Temp.: 241 C; RH: 7010% and photophase: 12 h

Treatment Adults test (n=6)

Parasitism rate (eggs/female)1

(meanSE)

PR2 Class3

Abamectin 0.00.00 b 100.0 4

Acetamiprid 0.40.18 b 98.3 3

Cartap 0.00.00 b 100.0 4

Chlorpyrifos 0.00.00 b 100.0 4

Control 23.16.92 a

Treatment Larvae test (n=8)

Emerged adults1

(meanSE)

PR2 Class3 Parasitism rate

(eggs/female)1

(meanSE)

PR2 Class3

Abamectin 63.21.56 a 12.8 1 11.41.92 b 72.6 2

Acetamiprid 70.80.33 a 2.3 1 36.32.70 a 12.7 1

Cartap 45.712.70 b 37.0 2 8.03.48 b 80.8 3

Chlorpyrifos 66.32.64 a 8.6 1 34.64.45 a 16.8 1

Control 72.50.86 a 41.66.93 a

Treatment Pupae test (n=7)

Emerged adults1

(meanSE)

PR2 Class3 Parasitism rate

(eggs/female)1

(meanSE)

PR2 Class3

Abamectin 70.915.46 b 26.3 1 4.92.22 b 82.6 3

Acetamiprid 91.01.05 a 5.4 1 12.05.60 b 57.3 2

Cartap 0.00.00 c 100.0 4

Chlorpyrifos 0.00.00 c 100.0 4

Control 96.21.33 a 28.12.30 a

1Figures followed by the same letter were not significantly different (p>0:05) by theScottKnott grouping analysis test.2Percentage reduction in parasitism rate or adult emergence compared to the control.3

Class=IOBC Classification.



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30% in the emergence of T. pretiosum; however, they reduced the

parasitism capacity of the emerged adults, with reduction of 82.6

and 57.3%, respectively, being observed int the parasitism rates.Abamectin was classified as moderately harmful, whereas acetamiprid

was slightly harmful. In the pupae test it was not possible to assess

the effects of the compounds cartap and chlorpyrifos on the parasit-

ism capacity this biological trait of T. pretiosum, because these pesti-

cides reduced in 100% the emergence of this egg parasitoid species.

Discussion and conclusion

The drastic reduction of parasitism by females exposed to fresh dry

residues of the evaluated insecticides was expected because com-

pounds belonging to the chemical groups of the lactones, carbamates,

neonicotinoids and organophosphates are related in the scientific

literature as highly harmful to parasitoids, important biological

control agents of arthropod pests (Croft, 1990; Yamamoto et al.,

1995; Hassan et al., 1998; Takahashi et al., 1998; Abdelgader and

Hassan, 2002; Carvalho et al., 2003; Moura et al., 2004, 2005). How-

ever, the effects of some compounds, mainly of neonicotinoids on

parasitoids belonging to the genus Trichogramma are less known.

The high mortality of adults observed in the emergence tubes

caused by the pesticides cartap and chlorpyrifos is not clear until this

moment. A similar effect was related by Abdelgader and Hassan

(2002) to mevinphos. However, these authors attributed the high mor-

tality observed in the inward of the cages to the high vapor pressure

of that pesticide.

The effect of the evaluated pesticides on the larval and pupalstages of the parasitoids was less harmful when compared to the adult

one. The likely reason is the higher susceptibility of the adult stage,

while the stages that occur inside its host are better protected and

therefore more tolerant.

The highest impact caused for cartap on the parasitoid emergence

from treated eggs containing the larval stage can be associated to the

capacity of this pesticide to penetrate through the host chorion,

affecting the parasitoid development (Guifen and Hirai, 1997; Schuld

and Schmuck, 2000; Consoli et al., 2001), or due to the ingestion ofresidues by the parasitoid during the opening of the emergence hole,

as also observed by Consoli et al. (2001).

The reduction in parasitism by females of T. pretiosum from treated

larvae stage with cartap within eggs of A. kuehniella might be due to



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their residual effect, causing high mortality of newly emerged females

(low longevity) and adversely affecting the number of eggs parasitized

per female. The effect caused by abamectin on T. pretiosum, however,can be associated to its mode of action, affecting its parasitism behav-

ior, because this pesticide did not affect the emergence of this parasit-

oid. Thus, females that maintained contact with residues of that

compound present in the host chorion had their parasitism capacity

reduced.

The effects of cartap and chlorpyrifos on the emergence of T. preti-

osum adults from treated host eggs containing the pupal stage of the

parasitoid might have been a result of the mortality of the wasps still

inside the host, due to the capacity of some pesticides to penetratethrough the host chorion. Just as observed for the larval stage of T.

pretiosum, abamectin and acetamiprid were harmless to this parasitoid

in the pupal stage.

Reductions in parasitism caused by abamectin and acetamiprid

indicate a residual effect of these pesticides on females from treated

eggs containing the pupal stage of T. pretiosum. In this case, residues

of these pesticides in the individuals might result in a lethal effect by

reducing the longevity of females, or even a sub-lethal effect by reduc-

ing its parasitism, causing both effects cause reduction in the parasit-

ism by these parasitoids.

Based on the variations observed in the tolerance of this egg para-

sitoid species to the evaluated pesticides, related to its several life

stages, the choice of the best time to apply these toxicants should be

considered, aiming to minimize the impact of these compounds on

this parasitoid in integrated pest management programs.

In conclusion, the adult stage of T. pretiosum is highly susceptible

to all insecticides evaluated in this study. Cartap is slightly harmful tolarvae while more harmful to pupae of this parasitoid wasp. Chlor-

pyrifos is harmful to the pupal stage of T. pretiosum, while abamectin

and acetamiprid are selective. Therefore, the use of abamectin and

acetamiprid could be recommended in association with T. pretiosum

in tomato pest management program.

Acknowledgements

The authors express their thanks to Raul N.C. Guedes and Rene

L.O. Rigitano for suggesting improvements to the initial manuscript,

and to Capes and CNPq for the scholarships awarded to the first

author.



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