J Pest Sci (2008) 81:49–55

DOI 10.1007/s10340-007-0184-7

ORIGINAL PAPER

EYcacy of inundative releases of Trichogramma evanescens in controlling Lobesia botrana in vineyards in Egypt

Nabil E. El-Wakeil · Hamza Th. Farghaly · Zakia A. Ragab

Received: 17 February 2007 / Revised: 2 October 2007 / Accepted: 4 October 2007 / Published online: 30 October 2007© Springer-Verlag 2007

Abstract The present work was conducted to evaluate theeYcacy of Trichogramma evanescens (Westwood) in con-trolling the European grape berry moth Lobesia botrana(Den. & SchiV.) in two vineyards, in El-Beheira and El-Gharbia Governorates, northern Egypt during the 2004 and2005 seasons. T. evanescens was mass produced onSitotroga cerealella (Olivier) eggs in National ResearchCenter in Egypt. The horizontal and vertical searchingactivity of T. evanescens was studied to determine theproper way of distributing the Trichogramma cards in vine-yards in 2004. Field experiments were also conducted toevaluate inundative releases of T. evanescens to controlL. botrana on large scale in 2005. Parasitism by T. evanes-cens on L. botrana eggs was greatly aVected with the hori-zontal or vertical distance from the release points.Parasitism reached over 97% and reduction percents ofinfestation were caused by the pest reached 96.8% intreated plots. A signiWcant increase in the crop wasachieved in treated plots. The results showed that therelease cards should be distributed in every three graperows and on height 130–170 cm to obtain good parasitismrates. T. evanescens could be a potential candidate for bio-logical control of L. botrana in vineyards.

Keywords Biological control · Field release · Lobesia botrana · Searching ability · Trichogramma · Vineyards

Introduction

Table grape is well known as a summer fruit in Egypt.The tortricid moth, Lobesia botrana (Den. & SchiV.) is akey pest of vineyards (Vitis vinifera) in many countries ofthe world. The moth is prevalent over a wide area inEurope and the Middle East (Louis and Schirra 2001), andit breeds three generations per year, causing considerablelosses in both quality and yield of grape. The second gen-eration shows up at the beginning of June and is wellknown under the name of “sourly worm” generation;however, the larvae still infest sour berries and the infes-tation prevents their maturation. The third generationstrikes the maturated clusters and therefore named “sweetworm” (Hillebrand and Eichhorn 1988). The damage tothe grape yield is twofold, direct damage by feeding lar-vae, and indirect damage by fungi and bacterial growth.The economic importance of L. botrana depends stronglyon the developmental stage of the grapevine (Louis andSchirra 2001). Before and during Xowering, the larvae atWrst penetrate single Xower buds, and later on they start totie together several Xower buds, building glomerules inwhich they stay and continue their feeding activities. Onthe other hand, the heaviest damage is in the second gen-eration. In this stage, the tolerance level for grape berrymoth infestation is relatively high and depends on theability of the grape variety to compensate the damage(Seaman et al. 1990; Ibrahim 2004).

The use of intensive insecticides to control L. botranain Egypt is causing many environmental problems as wellas increasing the resistance to this insect. Since excellentmethods for mass-rearing Trichogramma on factitioushosts are already known (El-Wakeil 2007), inundativereleases were considered as a possible alternative instead ofusing broad-spectrum insecticides to keep the environment

N. E. El-Wakeil (&) · H. Th. Farghaly · Z. A. RagabPests and Plant Protection Department, National Research Centre, Dokki, Cairo, Egypte-mail: n_emara@islamway.net

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clean. Under optimal conditions, the release of Tricho-gramma wasps can reduce damage caused by grape mothand give results equivalent to insecticide treatments(Nagarkatti et al. 2002). Remund and Bigler (1986)reported that as much as 90% parasitism of grape mothEupoecilia ambiguella by Trichogramma spp. in latesummer, but the build-up of the parasitoid was too slow tohelp in natural control of the pest (Seaman et al. 1990).Various Trichogramma species that have been consideredfor the biological control of lepidopterous pests have beenfound to be suYcient in their high searching ability, highfecundity, long survival and host preference (Fournier andBoivin 2000). Therefore, there were many attempts madeto control L. botrana and other lepidopterous grape pestswith augmentation of Trichogramma spp.: T. semblidis(Sengonca and Leisse 1987, 1989), T. dendrolimi, andT. maidis (Remund and Bigler 1986; Almatni et al. 2001),T. minutum, T. cacoeciae and T. evanescens (Hommayet al. 2002; Ibrahim 2004).

The searching activity of Trichogramma species isimportant in terms of developing eVective release tech-niques and for predicting the eYcacy of releases. One of theprime considerations in the development of biologicalcontrol is that the potential agent should have pronouncedhost-searching and dispersal abilities (McDougall and Mills1997). Searching vigor in many Trichogramma species hasevidently constrained the use of this genus in biologicalcontrol. In addition to being able to disperse rapidly, it isimportant that a biological control agent should remain inthe target area (Barnay et al. 2001; Hommay et al. 2002).

The present study was conducted to (1) study the search-ing activity of Trichogramma wasps in the vineyards of El-Beheira and El-Gharbia governorates in the 2004 season,(2) use these results to improve the impact of Weld releasesto control the target pest in commercial vineyards in the2005 season.

Materials and methods

Vineyards

Seedless grape trees, grown on lines 2 m between linesand 2 m between trees were used in these experiments.Two vineyards in northern Egypt, one in the El-BeheiraGovernorate (2 ha, sandy soil, 8-year-old trees), and theother in the El-Gharbia Governorate (1.25 ha, clay soil,10-year-old trees) were chosen for the present work. Inboth the farms, the grape trees were reared on three wiresvertically. In each farm, searching ability as well as theeYcacy of mass release of T. evanescens in controllingL. botrana throughout the 2004 and 2005 seasons wasstudied.

Searching ability of Trichogramma

Horizontal and vertical searching behavior of T. evanescenswas tested in Wve experimental plots in each farm in the2004 season to evaluate the searching ability in thesevineyards. The releases were repeated three times withintervals of 3 weeks. Release cards of the paper materialwith dimensions: 70 £ 50 £ 2 mm were used; a hole waspunched out. A self-adhesive label (11 £ 11 mm) with ca.1,000 parasitized Sitotroga eggs was introduced into thisframe.

In the horizontal searching behavior study

The releasing cards were hung in the middle of each ofthe seven trees in each plot. Each plot consisted of sevenvine rows (releasing row and the three neighboring rowsfrom each side) with along 100 m in each row (350 trees/plot), with 7 rows apart from each side between experi-mental plots, with rate of 50 cards/ha. The sample eggs(10/plot) were collected from every Wve vines from therelease row, the second three rows and from the neigh-boring three rows after 3 days post releases. The col-lected eggs were kept at 25 § 2°C and 70–80% RH and5 days later, the percentage of parasitism was deter-mined.

In the vertical searching behavior study

The grape trees were ca. 2.75 m high. The release cardswere hung on grape leaves at canopy level (130–170 cm)with rate of 50 cards/ha. Each plot consisted of 7 vine rowswith along 100 m (each row consists of 50 trees). Threedays later, the egg samples were taken at three various lev-els from the canopy (90–130, 130–170 and >170 cm). Thecollected eggs (10/plot) were kept at 25 § 2°C and 70–80%RH and 5 days later, the percentage of parasitism wasdetermined.

Mass release in vineyards

Mass release experiments were conducted in the 2005season in the El-Beheira and El-Gharbia governorates toevaluate the eYcacy of inundative releases ofTrichogramma parasitoids. Each farm was divided intothree experimental blocks (two release rates plus con-trol) with seven rows between treatments. Each experi-mental block was divided into four plots as replicates.Five releases of T. evanescens were applied at 2-weekintervals starting with Xowering stage at two releaserates (50 and 75 cards/ha). Releases were carried out on20 April, 5 May, 21 May, 5 June, and 20 June in El-Beheira, and on 4 May, 20 May, 3 June, 19 June, and 5

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J Pest Sci (2008) 81:49–55 51

July in El-Gharbia for controlling Lobesia with tworelease rates, 50,000 and 75,000 wasps/ha per eachrelease. Release cards with dimensions: 70 £ 50 £2 mm containing ca. 1,000 parasitized Sitotroga eggs/card were used. These cards were hung on grape leaf atthe middle level of the canopy (at 130–170 cm height)every four rows at a rate of 50 cards/ha, and every threerows at a rate of 75 cards/ha, based on the resultsobtained from the 2004 season.

Egg parasitism

The percentage of parasitism in L. botrana eggs byT. evanescens was determined by collecting samples of nat-ural pest eggs, which were found on ten trees in each plot(40 trees/treatment). Egg samples were collected from 4plots/treatment before release and 1and 2 weeks postrelease. Plant Xowers or buds with eggs were placed sepa-rately in vials after counting the eggs. The eggs were exam-ined daily under a binocular microscope and those hatchinginto larvae were recorded. Parasitized eggs were easilydetermined by their dark color and recorded.

Assessment of reduction percentages of infestation

After 4 weeks from the last release date, ten grape clusters/plot (40 clusters/treatment) were randomly examined fortortricid damage. The same number of clusters was alsoexamined in the control plot. Reduction percentages ofinfestation were determined based on grape clusters foreach treatment as compared to the control plots.

Larval population

At harvest time, the numbers of larvae were recorded froma sample of ten grape clusters/plot, which were randomlytaken from the released and control plots.

Yield assessment

To assess the yield, samples of grape clusters were ran-domly taken from 10 vines/plot after the grape reached amature stage; the mature grape was weighed to estimate theyield of 40 vines/treatment and the yield in kg/ha was cal-culated. The damaged clusters were also taken into consid-eration to estimate the grape yield.

Statistical analysis

The signiWcance in diVerences in the eYciency of Tricho-gramma was determined by an analysis of variance(ANOVA); then by LSD’s test. The signiWcance level forall analyses was P < 0.05 (Wilkinson et al. 2004).

Results

Searching ability of Trichogramma

Horizontal searching activity

The result in Fig. 1a shows the horizontal searching activityof T. evanescens from the release point; parasitism percent-ages were signiWcantly higher (df = 13; F = 44.78;P = 0.033) on the releasing row (97.2 and 95.9%), followedby direct three rows (78.3 and 75.4%) than on the neighbor-ing three rows (39.8 and 36.3%) in the El-Beheira andEl-Gharbia governorates, respectively. Parasitism activitydeclined gradually with increasing the distance from thereleasing point. The results showed that the release cardsshould be distributed in every 3–4 grape rows to achieve asuYcient control for the target pest.

Vertical searching activity

The middle height level (130–170 cm) of the canopy wasthe most active zone for Trichogramma searching abilityvertically. Parasitism dynamics diVered signiWcantly(df = 5; F = 67.23; P = 0.045) only between canopy levels

Fig. 1 Mean percentages of parasitism by Trichogramma evanescenson Lobesia botrana eggs in vineyard s in horizontal (a) (m) and vertical(b) (cm) direction, from release points

Heightes

90-130 cm130- 170 cm > 170 cm

)%(

msitisaraP

0

20

40

60

80

100

Distances

R. point 2m 4m 6m 8m 10m 12m

)%(

msitisaraP

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(B)

Parasitism % BE Parasitism % GH

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52 J Pest Sci (2008) 81:49–55

(130–170 and >170 cm); and it did not diVer signiWcantly(df = 5; F = 61.93; P = 0.075) between 90–130, and 130–170 cm, and also did not diVer signiWcantly (df = 5;F = 57.53; P = 0.118) between canopy levels (90–130 cmand >170 cm). Parasitism rates reached 91.5, 98.3, and89.3% in El-Beheira, and in El-Gharbia it reached 90.1,96.4, and 88.2% for height levels 90–130, 130–170 and>170 cm, respectively (Fig. 1b). The results obtained con-Wrmed that the height 130–170 cm is the best one to hangthe release cards of Trichogramma.

Mass-releasing Trichogramma in the vineyards

Parasitism rate

Data presented in Table 1 showed that parasitism rate washigher (df = 1; F = 68.21; P = 0.047) in El-Beheira than inthe El-Gharbia Governorate. It was also higher signiWcantly(df = 1; F = 63.32; P = 0.031) at the release rate of 75

cards/ha than at 50 cards/ha. The parasitism percentageswere 87.9 and 94.4% in the two release rates of 50 and 75cards/ha in El-Beheira Governorate, while in El-Gharbia,these percentages were 84.4 and 92.3 in the two releaserates, respectively. The signiWcant diVerences are betweenreleases rates inside each Governorate. At the beginning ofthe season, parasitism activity of nature Trichogramma waslow. Then, this activity increased with time to 24.8 and25.6% in El-Beheira and El-Gharbia Governorates, respec-tively.

Assessment of reduction percentages of infestation

Figure 2a presented that infestation rate by L. botrana washigher in El-Gharbia (13.6%) than in El-Beheira (10.2%).The release of Trichogramma showed that the lowest infes-tation rate was 3.2% at high release rate (75 cards/ha), fol-lowed by 7.0% at low release rate (50 cards/ha), while itwas 87% in control plots in the El-Beheira Governorate. In

Table 1 Mean numbers of eggs of Lobesia botrana /ten grape trees and parasitism by Trichogramma evanescens in El-Beheira and El-GharbiaGovernorates in 2005 season

C control, T50 50 Trichogramma cards/ha, T75 75 Trichogramma cards/ha

Treatment Measurements Experimental sites

El-Beheira El-Gharbia

C T 50 T 75 C T 50 T75

Before the Wrst release Egg masses Nr/10 Trees 36.0 § 0.31 32.0 § 0.33 37.0 § 0.36 40.0 § 0.41 38.0 § 0.39 39.0 § 0.42

Parasitized eggs (%) 9.0 § 0.11 9.8 § 0.12 9.9 § 0.13 9.9 § 0.12 10.2 § 0.13 10.6 § 0.15

One week after the 1st release

Egg masses Nr/10 Trees 39.0 § 0.40 32.0 § 0.34 30.0 § 0.31 43.0 § 0.45 42.0 § 0.46 30.0 § 0.31

Parasitized eggs (%) 11.5 § 0.13 76.8 § 0.89 93.8 § 1.21 11.9 § 0.13 70.7 § 0.76 88.9 § 1.25

Two weeks after the 1st release

Egg masses Nr/10 Trees 43.0 § 0.41 25.0 § 0.26 15.0 § 0.16 45.0 § 0.48 35.0 § 0.39 15.0 § 0.14

Parasitized eggs (%) 12.0 § 0.11 80.0 § 0.89 94.2 § 0.99 13.8 § 0.16 83.5 § 0.97 93.6 § 1.3

One week after the second release

Egg masses Nr/10 Trees 41.0 § 0.45 20.0 § 0.23 10.0 § 0.13 45.0 § 0.47 25.0 § 0.23 15.0 § 0.11

Parasitized eggs (%) 14.9 § 0.15 87.0 § 1.21 94.2 § 1.32 15.0 § 0.13 82.0 § 0.98 92.5 § 1.21

Two weeks after the second release

Egg masses Nr/10 Trees 38.0 § 0.41 18.0 § 0.13 9.0 § 0.13 40.0 § 0.50 20.0 § 0.21 15.0 § 0.17

Parasitized eggs (%) 18.9 § 0.17 93.8 § 1.23 93.1 § 1.14 19.2 § 0.21 87.5 § 0.98 93.6 § 1.1

One week after the third release

Egg masses Nr/10 Trees 27.0 § 0.28 13.0 § 0.16 7.0 § 0.11 30.0 § 0.43 15.0 § 0.13 10.0 § 0.20

Parasitized eggs (%) 21.6 § 0.23 89.7 § 1.23 97.0 § 1.31 22.0 § 0.24 85.7 § 1.07 95.0 § 1.25

Two weeks after the third release

Egg masses Nr/10 Trees 15.0 § 0.12 9.0 § 0.11 6.0 § 0.09 20.0 § 0.26 10.0 § 0.13 8.0 § 0.12

Parasitized eggs (%) 22.8 § 0.14 93.8 § 1.12 96.0 § 1.15 23.6 § 0.26 95.0 § 1.24 98.3 § 1.36

One week after the fourth release

Egg masses Nr/10 Trees 13.0 § 0.15 7.0 § 0.07 5.0 § 0.08 15.0 § 0.18 8.0 § 0.1 7.0 § 0.12

Parasitized eggs (%) 22.9 § 0.21 87.0 § 0.99 94.2 § 1.45 24.0 § 0.5 82.0 § 1.10 90.5 § 1.22

Two weeks after the fourth release

Egg masses Nr/10 Trees 9.0 § 0.1 6.0 § 0.07 3.0 § 0.04 10.0 § 0.12 6.0 § 0.08 5.0 § 0.07

Parasitized eggs (%) 23.9 § 0.21 93.8 § 1.20 93.1 § 1.24 24.2 § 0.26 87.5 § 0.98 90.6 § 0.95

One week after the Wfth release

Egg masses Nr/10 Trees 8.0 § 0.11 5.0 § 0.05 0.0 8.0 § 0.2 5.0 § 0.1 0.0

Parasitized eggs (%) 24.6 § 0.25 89.7 § 1.1 0.0 25.0 § 0.24 85.7 § 0.91 0.0

Two weeks after the Wfth release

Egg masses Nr/10 Trees 6.0 § 0.10 0.0 0.0 5.0 § 0.06 0.0 0.0

Parasitized eggs (%) 24.8 § 0.26 0.0 0.0 25.6 § 0.31 0.0 0.0

Mean Egg masses Nr/10 Trees 23.9 § 0.32 15.0 § 0.12 10.6 § 0.15 26.1 § 0.28 16.5 § 0.19 13.1 § 0.11

Parasitized eggs (%) 17.3 § 0.19 87.9 § 1.1 94.4 § 1.22 20.5 § 0.27 84.4 § 0.96 92.3 § 1.21

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J Pest Sci (2008) 81:49–55 53

the El-Gharbia Governorate the infestation rate was 4.4, 9.2and 92.4% in high, low release rates and control plots,respectively (Fig. 2a). This means that Trichogrammaachieved a reduction in grape moth infestation to 93.0 and96.8% in release rates of 50 and 75 cards/ha in El-Beheira;it was 90.8 and 95.6 in El-Gharbia, respectively.

Larval population

The mean of larvae population of L. botrana at harvest timewas 1.1 larvae/plot at high release rate (75 cards/ha), fol-lowed by 3.3 larvae/plot at low release rate (50 cards/ha),while it was 10 larvae/plot in control plots in the El-BeheiraGovernorate. In the El-Gharbia Governorate the larval pop-ulation was 1.6, 4.6 and 11.2 larvae/plot in high, lowrelease rates and control plots, respectively (Fig. 2b).

The yield

The grape yield in El-Beheira Governorate in the threetreatments was 23.0 tons/ha at release rate 75 cards/ha, fol-lowed by 21.5 tons/ha at rate 50 cards/ha, while it was 19.1tons/ha in control plots. In the El-Gharbia Governorate it

was 22.6, 21.4, and 18.9 tons/ha in high, low release ratesand control plots, respectively (Fig. 2c).

The considerable overall reduction in numbers of larvaein the treated plots compared to control plots appeared to beadequate enough to result in an increased yield. There wasa signiWcant diVerence (df = 5, F = 1152.72, P = 0.039) inthe yield of the released plots compared to the control plots.

Discussion

Trichogramma evanescens exhibit variable levels ofsearching either horizontally or vertically. Parasitism activ-ity declined gradually in the neighboring releasing rowsfrom the releasing point. These results are in agreementwith McDougall and Mills (1997) who found thatT. platneri released in apple orchards provided less than10% parasitism of sentinel egg masses 14 m away from therelease point. Also, Smith (1988) found that T. minutumparasitism declined with distance from a release point.

The present study indicated that at the middle heightlevel of the canopy (130–170 cm) was the zone of the high-est parasitism activity for Trichogramma. This may be dueto the distribution of the release cards at the middle of thecanopy (130–170 cm), or to the plant structure (plant/leafgrowth) at diVerent height levels, as reported by Lukian-chuk and Smith (1997). This result was agreed with Castan-eda-Samayoa et al. (1993) who tested the verticaldistribution of four Trichogramma species at the vine can-opy. He found that T. dendrolimi preferred the zone>150 cm height of canopy, while Yu et al. (1984) foundthat the vertical distribution of T. minutum within appletrees was skewed toward the lower pail of the tree canopy.The searching activity of the parasitoids is important interms of developing eVective release techniques and forpredicting the eYcacy of releases.

It is important to know how far from a release pointTrichogramma would reach so that an acceptable rate ofparasitism can be achieved. Therefore, searching activitycan be seen as a suitable trait for using biological controlagents, especially egg parasitoids as mentioned by Hassan(1993). As T. evanescens maximize their utilization ofeggs, proportion of eggs parasitized, there may be a beneWtto dispersing rapidly. Rapid searching may improve theirprobability of locating intact egg masses.

Trichogramma evanescens parasitizes a larger numberof eggs per L. botrana in high release rate (75 cards/ha)than the low one (50 cards/ha). Our results did not agreewith Fournier and Boivin (2000) who found no signiWcanteVect of release rate on T. pretiosum (Riley) and T. evanescens(Westwood) to control the economic insects. Activity ofTrichogramma was higher a little bit in El-Beheira than inEl-Gharbia. The limited development of vine foliage in

Fig. 2 Mean percentages of infestation a, numbers of L. botranalarvae b and grape yield c at diVerent treatments with Trichogrammaevanescens in El-Beheira (BE) and El-Gharbia (GH) Governorates.T75 Trichogramma 75 cards/ha; T50 50cards/ha. DiVerent letters indi-cate signiWcant diVerences

Treatments

T 75

ah/gK

d leiY

0

5000

10000

15000

20000

25000Yield BE Yield GH

)%(

noitatsefnI

0

20

40

60

80

100

Infestation % BE Infestation % GH

BB

C C

A Infestation (%)A

rN

eavraL

0

2

4

6

8

10

12

14

Larvae nr BE Larvae nr GH

AA

B

B

C

Laravae Numbers

C

YieldA A B B

C

T 50 Con

C

(A)

(B)

(C)

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54 J Pest Sci (2008) 81:49–55

El-Beheira Governorate may explain why T. evanescensparasitized grape moth eggs in this region more than in El-Gharbia Governorate, which enhanced Trichogrammawasps to move easily. This result is consistent with (Hom-may et al. 2002), who mentioned that development of vinefoliage aVected Trichogramma activity.

Natural parasitism of grape moth eggs by Tricho-gramma reached to average 17.3 and 20.5% in El-Beheiraand El-Gharbia Governorates. This result corresponds toBarnay (1999) and Ibrahim (2004), who stated that naturalparasitism of grape moth eggs by Trichogramma wasobserved in several places in vine-growing area, reachingup to 40 or 50%. The dynamics of parasitism in the vine-yard was related to the activity of L. botrana. This resultwas also in agreement with Sengonca and Leisse (1987)and Schade (1990) who found that the Trichogrammapopulation was very high in July, August and during earlyof September, takes into consideration that the weather inspring in Egypt is similar to the weather in summer inEurope.

The damage in the T. evanescens plots was greater atrelease rate of 50 cards/ha than at release rate of 75 cards/ha. Therefore, the eYcacy of T. evanescens appears to beimproved by about doubling the number of release cards.These results correspond to results reported by Castaneda-Samayoa et al. (1993) and Hommay et al. (2002).Zimmermann et al. (1997) released T. cacoeciae to con-trol Lobesia in vineyards and recorded reducing in infes-tation rates reaching up to 60%. T. evanescens wasleading at the average to reduction in infestation ratesreaching 96% in both El-Beheira and El-Gharbia govern-orates. The variation between T. evanescens eYcacy inboth governorates may be related to the development ofvine foliage or weather conditions. The weather in El-Beheira was hot and dry (mean temperature 36.7 andmean RH 66.3%); while in El-Gharbia it was warm andnot dry (mean temperature 32.2 and mean RH 74.1%);similar results were obtained by Wang et al. (1997) andFournier and Boivin (2000).

In the conclusion, the results showed that the releasecards should be distributed every three grape rows, alsothat the height 130–170 cm is the best height level to hangthe release cards to obtain the highest parasitism rates.The substantial overall reduction in infestation rates andnumbers of larvae in the released plots compared to con-trol plots, appeared to be adequate to result in increasedgrape yield. Increasing the grape yield in the treated plotsshould help the farmers to go ahead in mass releasingTrichogramma to produce the safe grape and earn moremoney. These results showed that T. evanescens could bepotential candidates for future mass rearing and Weldrelease programs for bio-control of L. botrana in vine-yards.

Acknowledgments We acknowledge the Wnancial support by NRC,Egypt (Project Nr. 7071104). We want to thank Prof. Dr. MahmoudSaleh for his helpful comments on the manuscript. We also appreciatethe owners of vineyards who allowed us to use their farms.

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