A laboratory test was conducted to determine the differential impact of insecticides on eggs of the brown stink bug, Euschistus heros (F.), and its parasitoid, Telenomus podisi Ashmead, in its immature phases inside the host egg, aiming to select those insecticides most toxic against the pest and harmless to the natural enemy. The bioassay was conducted at the Laboratory of Integrated Pest Management, Luiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba, SP, Brazil, from Jan to Aug 2023. The E. heros and T. podisi colonies, obtained initially from soybean crops (Piracicada, SP, Brazil, 22°50ʹ03ʹS, 48°01ʹ40ʹW), in Dec 2020, were reared in laboratory conditions at 70 ± 10% relative humidity, 25 ± 1 °C, and 14:10 L:D h cycle.

The ovicidal effect bioassay consisted of gluing 48-h-old E. heros eggs in rectangular cards (1.0 × 5.0 cm). Five cards with 60 ± 20 E. heros eggs per treatment were used. For the insecticide side-effect bioassay, couples of T. podisi were initially established and maintained for 24–36 h in glass vials (2.4 cm diameter × 8.0 cm height) containing pure honey as food for mating. Subsequently, 2 females (mated, fed, and without foraging experience with the host eggs) were transferred to a glass vial of the same size containing a drop of pure honey as food and an 18-h-old egg mass of E. heros (cards with 60 ± 20 E. heros eggs). The parasitism was allowed for 24 h. Two females for each card with 60 ± 20 E. heros eggs were used, totalizing 5 cards with 60 ± 20 E. heros eggs per treatment.

Eleven commercial insecticides were selected as treatments for both bioassays (ovicidal effect on E. heros and side effect on T. podisi). The design of this experiment was completely randomized with 11 treatments and 5 replications. The nonparasitized 48-h-old E. heros eggs and parasitized E. heros eggs at 72 h (“larval phase” of parasitoid inside the host) and 216 h (“pupal phase” of parasitoid inside the host) were treated with equivalent field rates of each insecticide adjusted to a volume of 200 L/ha. Thus, cards with eggs in the mentioned different times were completely immersed in the insecticide solution for 5 s. After the immersion, the treated eggs were placed onto paper towels and allowed to dry.

The insecticide effects on E. heros and T. podisi mortalities were assessed by the counting of E. heros-hatched nymphs and T. podisi-emerged adults from insecticide-treated eggs and compared among treatments with Kruskal–Wallis nonparametric analysis of variance using Dunn–Bonferroni post hoc test (P < 0.05). The mortality rates were also corrected for control using the Henderson and Tilton equation. Furthermore, a degree of differential toxicity was obtained by the ratio between the percentage of T. podisi emerged adults and the percentage of E. heros hatched nymphs. As an interpretation of these results, the higher value obtained means that the insecticide is concomitantly more toxic against the pest (E. heros) and more harmless to the natural enemy (T. podisi).

Results showed that insecticides Bold (fenpropathrin + acetamiprid), Maxsan (dinotefuran + pyriproxyfen), and Expedition (lambda-cyhalothrin + sulfoxaflor) provided the most significant ovicidal effects on brown stink bug, reducing the number of hatched nymphs by ≥85% (Tables 1 and 2). Except for Orthene (acephate) and Dimilin (diflubenzuron; “positive control”), all insecticides significantly reduced the egg parasitoid adults’ emergence when larvae and pupae inside the host were exposed to insecticides (Table 1). The less toxic effects for the larval phase of the egg parasitoid were achieved by Orthene, Pirephos (fenitrothion + esfenvalerate), Bold, and Expedition, whereas effects for the pupal phase were achieved by Orthene, Maxsan, Pirephos, and Bold, with mortality rates ≤35% (Table 2). According to the differential toxicity degree obtained (Table 2), the top 3 more toxic insecticides against the brown stink bug eggs and more harmless to the egg parasitoid were Bold, Maxsan, and Expedition.

Table 1.

Effect of insecticides on eggs of the brown stink bug, Euschistus heros (E.h.), and its egg parasitoid, Telenomus podisi (T.p.), immature stages

Treatment/formulationRate/haaE.h.T.p.
EggLarvalPupal
% hatched nymphsb% emerged adultsc
Acephate (Orthene)/75% (SP)1.0036.52a*63.04a77.18a
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5010.96c33.95c21.86c
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3014.50bc2.43e3.19d
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4015.70b37.92bc24.94c
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.000.68d0.48e22.66c
Fenitrothion + esfenvalerate (Pirephos EC®)/80 + 4% (EC)0.3535.08a54.30ab54.02b
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.900.40d49.64b50.12b
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0017.06b16.37d7.77d
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.307.08c41.83bc20.89e
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2017.28b31.20c18.82e
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.1459.20a51.86b67.52a
Control (distilled water) (“negative control”)50.10a64.90a71.60a
χ254.0347.1751.52
P<0.001<0.001<0.001
Treatment/formulationRate/haaE.h.T.p.
EggLarvalPupal
% hatched nymphsb% emerged adultsc
Acephate (Orthene)/75% (SP)1.0036.52a*63.04a77.18a
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5010.96c33.95c21.86c
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3014.50bc2.43e3.19d
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4015.70b37.92bc24.94c
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.000.68d0.48e22.66c
Fenitrothion + esfenvalerate (Pirephos EC®)/80 + 4% (EC)0.3535.08a54.30ab54.02b
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.900.40d49.64b50.12b
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0017.06b16.37d7.77d
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.307.08c41.83bc20.89e
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2017.28b31.20c18.82e
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.1459.20a51.86b67.52a
Control (distilled water) (“negative control”)50.10a64.90a71.60a
χ254.0347.1751.52
P<0.001<0.001<0.001

aField rate/hectare (L or kg of product/ha).

bOvicidal effect of insecticides on Euschistus heros.

cSide effect of insecticides on Telenomus podisi (larval phase: insecticide exposure at 72 h postparasitism; pupal phase: insecticide exposure at 216 h postparasitism).

*Means within a column followed by same letter are not statistically different (Dunn–Bonferroni test, P < 0.05).

Table 1.

Effect of insecticides on eggs of the brown stink bug, Euschistus heros (E.h.), and its egg parasitoid, Telenomus podisi (T.p.), immature stages

Treatment/formulationRate/haaE.h.T.p.
EggLarvalPupal
% hatched nymphsb% emerged adultsc
Acephate (Orthene)/75% (SP)1.0036.52a*63.04a77.18a
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5010.96c33.95c21.86c
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3014.50bc2.43e3.19d
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4015.70b37.92bc24.94c
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.000.68d0.48e22.66c
Fenitrothion + esfenvalerate (Pirephos EC®)/80 + 4% (EC)0.3535.08a54.30ab54.02b
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.900.40d49.64b50.12b
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0017.06b16.37d7.77d
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.307.08c41.83bc20.89e
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2017.28b31.20c18.82e
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.1459.20a51.86b67.52a
Control (distilled water) (“negative control”)50.10a64.90a71.60a
χ254.0347.1751.52
P<0.001<0.001<0.001
Treatment/formulationRate/haaE.h.T.p.
EggLarvalPupal
% hatched nymphsb% emerged adultsc
Acephate (Orthene)/75% (SP)1.0036.52a*63.04a77.18a
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5010.96c33.95c21.86c
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3014.50bc2.43e3.19d
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4015.70b37.92bc24.94c
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.000.68d0.48e22.66c
Fenitrothion + esfenvalerate (Pirephos EC®)/80 + 4% (EC)0.3535.08a54.30ab54.02b
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.900.40d49.64b50.12b
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0017.06b16.37d7.77d
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.307.08c41.83bc20.89e
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2017.28b31.20c18.82e
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.1459.20a51.86b67.52a
Control (distilled water) (“negative control”)50.10a64.90a71.60a
χ254.0347.1751.52
P<0.001<0.001<0.001

aField rate/hectare (L or kg of product/ha).

bOvicidal effect of insecticides on Euschistus heros.

cSide effect of insecticides on Telenomus podisi (larval phase: insecticide exposure at 72 h postparasitism; pupal phase: insecticide exposure at 216 h postparasitism).

*Means within a column followed by same letter are not statistically different (Dunn–Bonferroni test, P < 0.05).

Table 2.

Corrected mortality and differential toxicity for the brown stink bug, Euschistus heros (eggs) (E.h.), and egg parasitoid, Telenomus podisi (larval and pupal stages) (T.p.), after different insecticide exposures

Treatment/formulationRate/haaCM%bDifferential toxicitye
E.h.cT.p.dE.h.-egg × T.p.-larvalfE.h.-egg × T.p.-pupalg
EggLarvalPupal
Acephate (Orthene)/75% (SP)1.0026.940.300.001.732.11
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5077.9846.3583.023.101.99
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3070.9796.3795.650.170.22
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4068.0138.0467.352.421.59
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.0098.9799.2027.650.7133.32
Fenitrothion + esfenvalerate (Pirephos EC)/80 + 4% (EC)0.3529.3414.5024.871.551.54
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.9099.0824.1529.25124.10125.30
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0065.8973.9988.400.960.46
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.3085.6134.5070.595.912.95
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2065.5051.6174.301.811.08
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.140.0019.796.030.881.14
Control (distilled water) (“negative control”)
Treatment/formulationRate/haaCM%bDifferential toxicitye
E.h.cT.p.dE.h.-egg × T.p.-larvalfE.h.-egg × T.p.-pupalg
EggLarvalPupal
Acephate (Orthene)/75% (SP)1.0026.940.300.001.732.11
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5077.9846.3583.023.101.99
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3070.9796.3795.650.170.22
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4068.0138.0467.352.421.59
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.0098.9799.2027.650.7133.32
Fenitrothion + esfenvalerate (Pirephos EC)/80 + 4% (EC)0.3529.3414.5024.871.551.54
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.9099.0824.1529.25124.10125.30
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0065.8973.9988.400.960.46
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.3085.6134.5070.595.912.95
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2065.5051.6174.301.811.08
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.140.0019.796.030.881.14
Control (distilled water) (“negative control”)

aField rate/hectare (L or kg of product/ha).

bCorrected mortality (CM%) by Henderson–Tilton equation: CM% = {[1 − (n in Control before insecticide exposure * n in Treatment after insecticide exposure)/(n in Control after insecticide exposure * n in Treatment before insecticide exposure)]*100}.

cOvicidal effect of insecticides on Euschistus heros.

dSide effect of insecticides on Telenomus podisi (larval phase: insecticide exposure at 72 h postparasitism; pupal phase: insecticide exposure at 216 h postparasitism).

eDifferential toxicity = Percentage of Telenomus podisi adults emerged from immature stages (

flarval or

gpupal) exposed to insecticides/percentage of Euschistus heros hatched nymphs from eggs exposed to insecticides (data from Table 1).

Table 2.

Corrected mortality and differential toxicity for the brown stink bug, Euschistus heros (eggs) (E.h.), and egg parasitoid, Telenomus podisi (larval and pupal stages) (T.p.), after different insecticide exposures

Treatment/formulationRate/haaCM%bDifferential toxicitye
E.h.cT.p.dE.h.-egg × T.p.-larvalfE.h.-egg × T.p.-pupalg
EggLarvalPupal
Acephate (Orthene)/75% (SP)1.0026.940.300.001.732.11
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5077.9846.3583.023.101.99
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3070.9796.3795.650.170.22
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4068.0138.0467.352.421.59
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.0098.9799.2027.650.7133.32
Fenitrothion + esfenvalerate (Pirephos EC)/80 + 4% (EC)0.3529.3414.5024.871.551.54
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.9099.0824.1529.25124.10125.30
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0065.8973.9988.400.960.46
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.3085.6134.5070.595.912.95
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2065.5051.6174.301.811.08
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.140.0019.796.030.881.14
Control (distilled water) (“negative control”)
Treatment/formulationRate/haaCM%bDifferential toxicitye
E.h.cT.p.dE.h.-egg × T.p.-larvalfE.h.-egg × T.p.-pupalg
EggLarvalPupal
Acephate (Orthene)/75% (SP)1.0026.940.300.001.732.11
Alpha-cypermethrin + acetamiprid (Fastac Duo)/10 + 20% (SC)0.5077.9846.3583.023.101.99
Bifenthrin + acetamiprid (Sperto)/25 + 25% (WG)0.3070.9796.3795.650.170.22
Bifenthrin + imidacloprid (Galil SC)/25 + 5% (SC)0.4068.0138.0467.352.421.59
Dinotefuran + pyriproxyfen (Maxsan)/10 + 2.5% (EW)1.0098.9799.2027.650.7133.32
Fenitrothion + esfenvalerate (Pirephos EC)/80 + 4% (EC)0.3529.3414.5024.871.551.54
Fenpropathrin + acetamiprid (Bold)/7.5 + 11.2% (EW)0.9099.0824.1529.25124.10125.30
Lambda-cyhalothrin + dinotefuran (Zeus)/8.4 + 4.8% (EW)1.0065.8973.9988.400.960.46
Lambda-cyhalothrin + sulfoxaflor (Expedition)/10 + 15% (SE)0.3085.6134.5070.595.912.95
Lambda-cyhalothrin + thiamethoxam (Engeo Pleno S)/14.1 + 10.6% (SC)0.2065.5051.6174.301.811.08
Diflubenzuron (Dimilin)/25% (WP) (“positive control”)0.140.0019.796.030.881.14
Control (distilled water) (“negative control”)

aField rate/hectare (L or kg of product/ha).

bCorrected mortality (CM%) by Henderson–Tilton equation: CM% = {[1 − (n in Control before insecticide exposure * n in Treatment after insecticide exposure)/(n in Control after insecticide exposure * n in Treatment before insecticide exposure)]*100}.

cOvicidal effect of insecticides on Euschistus heros.

dSide effect of insecticides on Telenomus podisi (larval phase: insecticide exposure at 72 h postparasitism; pupal phase: insecticide exposure at 216 h postparasitism).

eDifferential toxicity = Percentage of Telenomus podisi adults emerged from immature stages (

flarval or

gpupal) exposed to insecticides/percentage of Euschistus heros hatched nymphs from eggs exposed to insecticides (data from Table 1).

Conflict of interest

This research was part of the routine pesticide screening work of the Laboratory of Integrated Pest Management (ESALQ-USP). No special research funds were allocated for this work.

This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected]
Section Editor: Michelle Brown
Michelle Brown
Section Editor
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