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Ecotoxicology

https://doi.org/10.1007/s10646-018-1954-0

1 Lethal and sublethal effects of insecticides on Engytatus varians


2 (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera:
3 Gelechiidae)
4 Daniel Alberto Pérez-Aguilar1 Marianne Araújo Soares2 Luis Clepf Passos2 Ana Mabel Martínez1
● ● ● ●

5 Samuel Pineda1 Geraldo Andrade Carvalho2


6 Accepted: 31 May 2018


7 © Springer Science+Business Media, LLC, part of Springer Nature

8 Abstract
9 The mirid Engytatus varians (Distant) is a promising biological control agent of the tomato borer, Tuta absoluta (Meyrick)
10 (Lepidoptera: Gelechiidae), one of the most destructive pests of tomato (Solanum lycopersicum L.). The effects of five
11
Q1
insecticides commonly used on tomato crops in Brazil were evaluated on E. varians in laboratory and semifield conditions.
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Glass Petri dish with residues of chlorfenapyr, thiamethoxam, and abamectin caused ˃90% mortality in both stages of the
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12
13 predator 72 h post-treatment, except imidacloprid that caused 78% of nymphs mortality. Teflubenzuron caused 24 and 66%
14 mortality on adults and nymphs, respectively. The offspring of females derived from treated nymphs with teflubenzuron was

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15 significantly lower than the control but not when females were treated as adults. Longevity of males derived from nymphs

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16 treated with teflubenzuron was significantly reduced, but no effects were observed on females. When males and females
17 were treated as adults with teflubenzuron there were no effects on their longevity. In the greenhouse-aged tomato plants, the
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18 2 h-old residues of thiamethoxam, chlorfenapyr, and abamectin caused more than 70% of mortality of third instar of E.
19 varians at 72 h post-treatment, 12 day-old residues of all three compounds caused a mortality lower than 30%. These data
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20 suggest that teflubenzuron can be associated with releases of E. varians adults, while the use of other evaluated pesticides
21 should be avoided in this situation. Although, the low persistence of these products indicate that their spraying and later
22 releases of E. varians adults on tomato crops are a possible strategy to control T. absoluta.
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23 Keywords Tomato crops Pest Biological control Pesticides Selectivity


● ● ● ●
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24 Introduction countries (Desneux et al. 2010, 2011; Campos et al. 2017; 30


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Sankarganesh et al. 2017; Sylla et al. 2017; Xian et al. 2017; 31


25 The tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Biondi et al. 2018). The caterpillars of this species feed on 32
26 Gelechiidae), is the most important pest of tomato crops the leaves, stems, flowers and fruits causing severe damage 33
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27 (Desneux et al. 2010). Native to South America, this pest is on tomato crop. After hatching, the larvae penetrate the 34
28 present in several parts of Europe, Africa, the Middle East leaves and consume the mesophyll creating conspicuous 35
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29 and parts of Asia with risks of outbreaks at the bordering mines, which affect the plant’s photosynthetic capacity. In 36
tomato stems, the larvae form galleries in the leaflets
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37
insertion, causing damage to future inflorescences (Tropea 38
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* Marianne Araújo Soares


Garzia et al. 2012). Tomato fruits can be damaged as soon 39

marianne_bio@hotmail.com as they are formed. When control measures are not adopted, 40
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T. absoluta can cause losses between 80–100% on tomato 41


1
Instituto de Investigaciones Agropecuarias y Forestales, crop (Desneux et al. 2010; Urbaneja et al. 2012).
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42
Universidad Michoacana de San Nicolás de Hidalgo, Km. 9.5
In Brazil, the use of insecticides is the main strategy to 43
Carretera Morelia-Zinapécuaro, Tarímbaro, Michoacán 58880,
Mexico control T. absoluta, with a great diversity of insecticide 44
2 classes commonly used, such as carbamates, neonicoti- 45
Departamento de Entomologia, Laboratório de Ecotoxicologia de
Inseticidas, Universidade Federal de Lavras, Caixa Postal 3037, noids, pyrethroids, avermectins, spinosyns, diamide and 46
Lavras, MG CEP 37200-000, Brazil insect growth regulators (MAPA 2017). However, T. 47
D. A. Pérez-Aguilar et al.

48 absoluta has high capacity to develop resistance towards the insecticides commonly used on tomato crops in Brazil on 101
49 majority of conventional compounds, therefore the control nymphs and adults of E. varians. 102
50 achieved by the insecticides might not be successful
51 (Siqueira et al. 2000a, b, 2001; Campos et al. 2014; Sohrabi
52 et al. 2016; Roditakis et al. 2017). In addition, excessive use Materials and methods 103
53 of chemical insecticides affects natural enemies, results in
54 secondary pest outbreaks and leads to other environmental Insects and pesticides 104
55 and human health damages (Margni et al. 2002; Abdollahi
56 et al. 2004). The larvae of T. absoluta are a difficult target The E. varians colony was initiated with ~200 adults col- 105
57 because they live inside plant tissues, which demand a high lected from open field of untreated tobacco plants in Lavras 106
58 number of applications on tomato fields (Guedes and (21°8.5960’S and 045°3.4660’W, 808 m of altitude) in the 107
59 Picanço 2012). state of Minas Gerais, Brazil. After being collected, insects 108
60 The zoophytophagous predators from the families Mir- were transported to the Laboratory of Ecotoxicology of the 109
61 idae and Anthocoridae are important natural enemies in Federal University of Lavras and identified on the basis of 110
62 agricultural systems and are often effective against arthro- visual morphological characters according to the key of 111
63 pod pests such as whiteflies, aphids, thrips, mites and mirid species proposed by Ferreira and Henry (2011). Once 112
64 lepidopterans (Urbaneja et al. 2012; Zappalà et al. 2013; in the laboratory, insects were transferred to one of three 113
65 Mollá et al. 2014; Perdikis and Arvaniti 2016; Salehi et al. acrylic boxes (60 × 30 × 30 cm) containing a tobacco plant 114
66 2016). Macrolophus pygmaeus Rambur and Nesidiocoris (cv. TNN) (30 cm in height with four to six fully expanded 115
67 tenuis Reuter (Hemiptera: Miridae) are native to the Med- leaves) per box as oviposition substrate and water source. 116
68 iterranean basin and are commercially mass produced and Nymphs and adults of E. varians were fed with Ephestia 117
69 successfully released on tomato and other vegetables crops kuehniella (Zeller) (Lepidoptera: Pyralidae) eggs (Insecta 118
70 alone (Calvo et al. 2012) or in combination with insecticidal Agentes Biológicos, Lavras, MG, Brazil), which were 119

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71 compounds (Mollá et al. 2011; Zappalà et al. 2012). In sprinkled on the tobacco leaves. Every seven days new 120

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72 South America, research with T. absoluta predators has tobacco plants were used to sustain the predator colony and 121
73 only started recently. High predation rates were recorded by the plants containing eggs were transferred to an insect free 122
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74 three mirid bug species, including Engytatus varians (Dis- cage. The predator rearing was maintained in a climate 123
75 tant) (Hemiptera: Miridae). This predator can be found in controlled room at 25 ± 2 °C, 70 ± 10% relative humidity, 124
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76 Brazil, Cuba and Mexico (Castineiras 1995; Bueno et al. and a photoperiod of 12:12 h (L: D). 125
77 2013; Martínez et al. 2014; Silva et al. 2016). E. varians is The insecticides tested were chlorfenapyr, thiametoxam, 126
78 able to prey T. absoluta eggs, consuming 392.8 in the abamectin, imidacloprid and teflubenzuron, at the maximum 127
nymphal stage and an average of 92 per day in the adult recommended dosage to pest control on tomato crops in
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79 128
80 stage, thus it is a promising biological control agent (Bueno Brazil (Table 1). Distilled water was used as the control 129
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81 et al. 2013; Van Lenteren et al. 2017). treatment. 130


82 In integrated pest management programs, the compat-
83 ibility of insecticides and natural enemies is a critical point Lethal and sublethal effects on nymphs and adults 131
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84 of success (Biondi et al. 2012a, b, 2013), thus it is important in laboratory trials 132
85 to evaluate how these products affect the efficacy of bene-
86 ficial insects (Abbes et al. 2015; Bueno et al. 2017). It is Nymphs and adults of E. varians were exposed to fresh 133
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87 well known that the natural enemies, like predators, are residues of insecticides in Petri dishes (10 cm diameter × 134
88 more susceptible to pesticides, not only in mortality that 1.5 cm height). The dishes were treated in a Potter Precision 135
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89 some compounds can cause to these arthropods, but also in Tower (Burkard Scientific Co., Uxbridge, UK, calibrated 136
the side-effects on the physiology and behavior, which may pressure: 100 kPa) with an application volume of 1.5 ± 0.5
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90 137
91 have significant consequences on life parameters and affect μL/cm2 per Petri dish. 138
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92 the efficiency of natural enemies (Desneux et al. 2007; These bioassays were performed under the same 139
93 Guedes et al. 2017). laboratory conditions described above and based on the 140
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94 The frequent pesticide use on tomato crops in South methodology described by Arnó and Gabarra (2011) for the 141
America might compromise the success of the predatory predators M. pygmaeus, N. tenuis, and Orius laevigatus
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95 142
96 mirids. Before considering E. varians releases on tomato Fieber (Hemiptera: Anthocoridae). Once the plates were dry 143
97 crops, it is necessary to assess how pesticides affect this (1.5 h after treatment), ten E. varians third instar nymphs or 144
98 predator. Therefore, the objective of this study was to ten adults (5 females + 5 males, <3 d old) (=one replicate) 145
99 evaluate the lethal (direct mortality) and sublethal (adult were placed into each Petri dish. A little tobacco leaf 146
100 longevity and offspring) effects of five conventional (approximately 3 cm diameter) was added as water source 147
Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator. . .

for the insects. The leaf petiole was wrapped in a piece of


% a.i. Rate ha−1
174
173
172
171
170
169
168
167
166
165
164
163
162
161
160
159
158
157

100 mL
200 mL
50 mL

50 mL
moist cotton to prevent dehydration. As food source, 0.2 g 175

20 g
of E. kuehniella eggs were placed on the bottom of the Petri 176
dishes. Both tobacco leaf and E. kuehniella eggs were 177

1.8
replaced every 48 h. The Petri dishes were covered with an
Uncouplers of oxidative phosphorylation via disruption of the proton gradient 24
25

48
15
178
organdy mesh screen held in place with a rubber band to 179
allow air circulation and to prevent the insects from 180
escaping. The mortality of nymphs and adults was checked 181
at 24 h intervals for a period of 3 days after they were 182
placed on treated Petri dishes. Insects were considered dead 183
when they were touched with a thin bristle brush and no 184
movement was observed. Eight replicates per each treat- 185
GABA- and glutamate-gated chloride channel agonist

ment and per each life stage were carried out. 186
Nicotinic acetylcholine receptor (nAChR) agonists

Nicotinic acetylcholine receptor (nAChR) agonists

After three days of treatment, surviving nymphs and 187


adults were removed from treated Petri dishes and the 188
sublethal effects on offspring (number of emerged nymphs/ 189
female) and adult longevity were assessed in treatments, 190
where at least 30% of surviving nymphs or adults were 191
Inhibitors of chitin biosynthesis
Table 1 Insecticides, active ingredients, concentrations, and manufacturers used for effects on Engytatus varians in this study

obtained from the residual contact bioassay described 192


above. For this, surviving nymphs were transferred to 193
untreated Petri dishes containing a tomato leaf and supplied 194
with E. kuehniella eggs (0.2 g replaced every 48 h for all 195
Chemical group Mode of action

treatments, as described above). Development of these 196

F
nymphs was followed until adulthood. 197

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The effect of insecticides on offspring was also eval- 198
uated. For this, a tomato plant (~20 cm height with two to 199
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three expanded leaves), grown in a plastic cup (50 mL) 200
containing a mixture of compost and peat substrate (1:1),
Water dispersible granule Neonicotinoid

Imidacloprid Nortox® (Nortox) Concentrated suspension Neonicotinoid

201
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Concentrated suspension Benzoylurea
Concentrated suspension Avermectin

was enclosed in a cylindrical plastic tube (9 cm diameter × 202


24 cm height) opened at both ends. The top of the cylinder
Concentrated suspension Pyrrole

203
was covered with a fine mesh screen to allow air circulation 204
and to prevent escape of the insects. One couple of adults
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205
(<3 d old) derived from surviving nymphs (generation F1) 206
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was placed into each cylinder. E. kuehniella eggs were 207


spread on tomato leaves. Each pair was transferred to a new 208
cylinder with food and one new tomato plant every 48 h
Formulation

209
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until their death. Previously, Pineda et al. (2016) reported 210


that the duration of E. varians egg stage was 9.2 days 211
(ranged from 8 to 11 days); for this reason, to register the 212
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number of emerged nymphs/female in each treatment, 213


tomato plants were checked daily from 7th to 14th days 214
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after oviposition. To record longevity, adults were checked 215


Active ingredient Trade name (supplier)

Vertimec® (Nortox)

every 24 h until death. Ten replicates per each treatment,


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Actara® (Syngenta)

216
each consisting of a couple of E. varians, were used.
Nomolt® (Basf)

217
Pirate® (Basf)

The same procedure was applied to adults exposed to 218


pesticide residues in Petri dishes. After evaluation of sur- 219
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vival, the surviving adults of E. varians were removed from 220


the treated Petri dishes and they were immediately placed in
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221
couples on tomato plant as described above. The rest of the 222
Thiamethoxam

Teflubenzuron
Chlorfenapyr

bioassay was similar to the procedure described to assess


Imidacloprid

223
Abamectin

the sublethal effects on adults derived from surviving 224


nymphs. 225
D. A. Pérez-Aguilar et al.

226 Persistence trials in semifield conditions Abbott’s formula (Abbott 1925): 276
 
Mt  Mc
227 To determine the initial toxicity and persistence of insecti- Ma ¼100 
100  Mc
228 cide residues in greenhouse conditions, the methodology
229 used in this bioassay was based on the semifield tests where Ma = corrected mortality, Mt = treatment mortality, and 277
278
279
280
230 described by Van De Veire et al. (2002) with some mod- Mc = control mortality. Treatments in which offspring was 281
231 ifications. Tomato plants (~20 cm height with 3 fully evaluated, the values were corrected according to the equation: 282
232 expanded true leaves) were treated using a handheld
Fx 100
233 sprayer until runoff (~6 mL) with the maximum field Efx ¼ 100 
FC
234 recommended concentration of insecticides that caused
235 high mortalities to E. varians nymphs and adults in the where Fx is the mean predator reproductive capacity for 284
283
286
285
236 previous experiments (classes 3 and 4), according to IOBC pesticide x and Fc is the predator reproductive capacity 287
237 guidelines. Control plants were sprayed with distilled water recorded in the control treatment. In these cases, the total 288
238 only. reduction coefficient was provided using the formula: 289
239 Treated plants were left to dry (1.5 h after treatment) in a    
Ma Efx
240 ventilated greenhouse located on the campus of Federal EX ¼ 1  1  1
100 100
241 University of Lavras. The temperature of this greenhouse
242 was ∼25 °C, ∼40 RH, and natural photoperiod of 12: 12 (L: where Ma is the corrected mortality and Efx is the corrected 292
291
290
243 D). Insects were exposed to treated plants at two different predator reproductive capacity estimated using the metho- 293
244 aged residues: 2 h and 12 d after the application of the dology described by Biondi et al. (2012a, b). 294
245 products. Each replicate consisted of a tomato plant and ten The values Ma or Ex (if available) were then classified 295
246 third instar nymphs of E. varians placed into an and interpreted according to the standards of the Interna- 296
247 acrylic frame box (60 × 40 × 40 cm) covered with a tional Organization for Biological Control (IOBC) which 297

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248 cotton organdy fabric in its upper gap to ensure adequate include four classes: (1) harmless: <30%, (2): slightly 298

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249 ventilation. The predator nymphs were fed ad libitum harmful: 30–79%, (3): moderately harmful: 80–99%, and 299
250 with E. kuehniella eggs as described above. Four (4): harmful:>99%. 300
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251 plants were used for each insecticide and control on each
252 date.
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253 We used a randomized block design with four treatments Results 301
254 and four replicates in each date. Mortality of nymphs was
255 assessed at intervals of 24, 48 and 72 h after they were Lethal effects on nymphs and adults in laboratory 302
placed on treated tomato plants. Insects were considered
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256
257 dead when they were touched with a thin bristle brush and Engytatus varians nymphs were susceptible to fresh resi- 303
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258 no movement was observed. dues in glass Petri dishes of the five insecticides (Table 2). 304
259 To classify the pesticides according to their persistence to At 24 h post-treatment, mortality ranged between ~17 and 305
260 E. varians nymphs, the persistence categories proposed by 84% for all compounds and all of them were significantly 306
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261 IOBC/WG “Pesticides and Beneficial Organisms” tests different from control (F5,42 = 43.35, p < 0.01). At 48 h 307
262 were used: class A = short lived (<5 days), B = slightly post-treatment, the cumulative mortality caused by aba- 308
263 persistent (5–15 days), C = moderately persistent mectin, imidacloprid, thiamethoxam, and chlorfenaphyr was 309
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264 (16–30 days), and D = persistent (>30 days) (Sterk et al. >80%, whereas at 72 h post-treatment it was >90%. At 48 310
265 1999). (F5,42 = 48.49, p < 0.01) and 72 h post-treatment (F5,42 = 311
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89.27, p < 0.01), all insecticides were noxious. At these 312


Data analysis times, teflubenzuron caused significantly lower mortality
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266 313
compared to the remained treatments. Mortality in the 314
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267 General linear models were fitted according to mortality control never exceeded 5%. 315
268 caused by the products in laboratory and persistence The susceptibility of E. varians adults depended on the 316
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269 bioassays, and the treatments were compared by analysis of type of insecticide being used (Table 3). At 24 h post- 317
aggregation levels, using the statistical software R (R Core treatment, the mortality caused by thiamethoxam, imida-
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270 318
271 Team 2016). The number of nymphs/female and longevity cloprid, and chlorfenaphyr ranged between 40 and 70% and 319
272 data were analyzed by Student t test, or where not normally all of them were significantly different from that observed in 320
273 distributed, by the non-parametric Mann-Whitney U test. abamectin, teflubenzuron, and control (≤6%) (F5,42 = 37.65, 321
274 The mortality caused by the products was corrected to the p < 0.01). At 48 and 72 h post-treatment, however, the 322
275 mortality caused in the control treatment according to the cumulative mortality caused by abamectin, thiamethoxam, 323
Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator. . .

Table 2 Effects of five


Treatment Third instar mortality (%) (time after Ma (%)a Efxb Exc IOBC Toxicity Classd
insecticides on third instar of
application)
Engytatus varians after
continuous exposure to fresh 24 h 48 h 72 h
residue in glass Petri dishes
Control 2.5 ± 1.63a 3.75 ± 1.82a 5.0 ± 1.88a – – – –
b b
Teflubenzuron 17.5 ± 2.5 43.75 ± 4.9 66.25 ± 4.19b 64.47 44.13 80.00 3
Abamectin 21.25 ± 3.98b 82.5 ± 6.47c 92.5 ± 2.5c 92.11 – – 3
Imidacloprid 51.25 ± 6.92c 81.25 ± 4.79c 93.75 ± 2.63c 93.42 – – 3
Thiamethoxam 65.0 ± 3.27 c c
86.25 ± 4.60 91.25 ± 2.95 c
90.79 – – 3
Chlorfenapyr 83.75 ± 4.60d 100.0 ± 0.0d 100.0 ± 0.0d 100 – – 4
Means within columns followed by the same letter are not significantly different (P < 0.05)
Class 1: harmless (<30%); Class 2: slightly harmful (30%–79%); Class 3: moderately harmful (80%–99%);
Class 4: harmful (>99%)
a
Corrected mortality
b
Effect on offspring
c
Total reduction coefficient
d
IOBC toxicology classes considering Ma or Ex (if available)

Table 3 Effects of five


Treatment Adult mortality (%) (time after application) Ma (%)a Efxb Exc IOBC toxicity classd
insecticides on Engytatus
varians adults, after continuous 24 h 48 h 72 h
exposure to fresh residue in
glass Petri dishes Control 1.25 ± 1.25 a
5.00 ± 2.67 a
6.25 ± 1.82a – – – –
a b b
Teflubenzuron 6.25 ± 2.63 22.50 ± 5.90 24.28 ± 7.25 19.23 24.51 40.00 2

F
Imidacloprid 41.21 ± 3.98b 58.75 ± 6.92c 78.25 ± 5.15c 76.80 – – 2

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Abamectin 5.00 ± 2.67a 80.00 ± 5.97d 92.50 ± 3.13c 92.00 – – 3
Thiamethoxam 40.00 ± 3.77b 82.50 ± 6.92d 95.00 ± 3.27c 94.67 – – 3
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Chlorfenapyr 70.00 ± 5.60c 98.00 ± 1.25e 100 ± 0.00d 100.00 – – 4
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Means within columns followed by the same letter are not significantly different (P < 0.05)
Class 1: harmless (<30%); Class 2: slightly harmful (30–79%); Class 3: moderately harmful (80%–99%);
Class 4: harmful (>99%)
a
Corrected mortality
D

b
Effect on offspring
c
Total reduction coefficient
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d
IOBC toxicology classes considering Ma or Ex (if available)
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324 and chlorfenapy ranged between 80 and 100%, while imi- compared with control treatment (t = 3.27, p < 0.01) 339
325 dacloprid caused 58.75 and 78.25% mortality in both dates. (Table 4). Females derived from nymphs treated with 340
326 At 48 and 72 h post-treatment, the mortality caused by teflubenzuron produced less offspring. 341
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327 teflubenzuron on E. varians adults was 22 and 24%, Teflubenzuron significantly reduced the longevity of 342
328 respectively, which were significantly different from the males (t = 3.91, p < 0.01) but not of females (t = 1.41, p = 343
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329 results obtained by the remaining compounds and the 0.17) of E. varians derived from exposed nymphs to the 344
control (F5,42 = 35.38, p < 0.01 and F5,42 = 50.00, p < 0.01 compound. There was no difference between longevity of
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330 345
331 for 48 and 72 h post-treatment, respectively). males and females, in both treatments (control: t = −1.51, 346
C

332 According to mortality criteria established by the IOBC, p = 0.14; teflubenzuron: t = 1.12, p = 0.27). No significant 347
333 chlorfenapyr was classified as the highest in toxicity (class differences were observed in the number of nymphs/female 348
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334 4), followed by thiamethoxam and abamectin (class 3), (U = −22.0, p = 0.10) derived from surviving adults 349
imidacloprid and teflubenzuron (class 2) (Table 3). exposed to teflubenzuron compared to adults exposed to
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335 350
untreated control. Teflubenzuron did not affect the long- 351
336 Sublethal effects on nymphs and adults evity either of males (t = 0.64, p = 0.52) and females (t = 352
1.25, p = 0.22) or intra sex (t = −0.27, p = 0.78 and t = 353
337 Significant differences were observed in the offspring of −0.88, p = 0.38) for comparisons between males and 354
338 adults derived from nymphs treated with teflubenzuron females in control and teflubenzuron, respectively (Table 4). 355
D. A. Pérez-Aguilar et al.

Table 4 Adult longevity and


Treatment Adult longevity (days) Offspring (nymph/female)
offspring from nymphs and
adults of Engytatus varians Male Female
treated with insecticides
Treated nymphs assay
Control 36.4 ± 3.82Aa 29.3 ± 2.73Aa 70.7 ± 6.50A
Teflubenzuron 18.8 ± 2.36Ba 23.3 ± 3.2Aa 39.5 ± 6.95B
Treated adults assay
Control 34.1 ± 3.86Aa 32.7 ± 3.33Aa 66.1 ± 6.18A
Teflubenzuron 30.9 ± 1.5Aa 27.0 ± 3.08Aa 49.9 ± 8.25A
Means within columns (capital letter) and within lines (lower letter) followed by the same letter are not
significantly different for adult longevity and means within columns (capital letter) are not significantly
different for offspring (ANOVA, LSD; P > 0.05)

Table 5 Statistic from the GLM used to analyze the mortality of The interaction between mortality and residue age at 48 h 374
Engytatus varians nymphs in the persistence test in two dates of
and 72 h after contact with residues illustrates that time of 375
evaluation (2-h and 12-day post-pesticide spraying in tomato plants)
after 24, 48 and 72 h in contact with pesticides residues exposure affects the mortality caused by products, which 376
increased over time. Regarding the residues ages (2-h and 377
Source of variation Degrees of freedom F p-value
12-day), a decrease in mortality caused by the products was 378
24 h observed in all evaluation times (24, 48 and 72 h), 379
Mortality 3 11.38 <0.01 demonstrating the reduction of pesticide activity with time. 380
Date 1 6.43 0.02 Considering the mortality caused by the products after 72 h 381

M×D 3 0.94 0.44 of exposure residues for each residue age, all evaluated 382

F
48 h compounds were classified as class B (slightly persistent), 383

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Mortality 3 20.87 <0.01 according to persistence criteria established by the IOBC. 384

Date 1 71.45 <0.01


O
M×D 3 7.27 <0.01
Discussion 385
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72 h
Mortality 3 37.02 <0.01
The evaluated insecticides showed different degrees of 386
Date 1 145.20 <0.01
toxicity to E. varians in laboratory conditions, with differ- 387
M×D 3 11.42 <0.01
ences being also highlighted between the developmental
D

388
stages of the predator, as has been also reported in other 389
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studies (Biondi et al. 2015; Prabhaker et al. 2017). Chlor- 390


356 Semifield test of persistence fenapyr showed higher toxicity to nymphs and adults when 391
compared with the other insecticides. It is an insecticide that 392
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357 After 24 h of exposure to pesticides residue on tomato acts in the synthesis of ATP in the mitochondria, resulting 393
358 plants, all evaluated products were similar and different in cell death and causing quickly lethal effect on insects 394
359 from control in both residues ages (Table 5, Fig. 1). The (Rust and Saran 2006). Similarly, this compound showed 395
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360 mortality caused by thiamethoxan and chlorfenapyr in 2-h high toxicity to other hemipteran predators, such as Mac- 396
361 residue was significantly higher than the 12-day residue, rolophus basicornis (Hemiptera: Miridae) (Passos et al. 397
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362 while abamectin caused similar mortality in both residues 2017), Orius tristicolor (White), Amphiareus constrictus 398
ages. In the next evaluation (48 h), the mortality caused by (Stal) and Blaptostethus pallescens Poppius (Hemiptera:
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363 399
364 all pesticides differed from the control in both residues ages. Anthocoridae) (Pereira et al. 2014). 400
C

365 The mortality was significantly higher between the first and It was observed that imidacloprid and thiamethoxam 401
366 second ages for all pesticides. After 72 h of evaluation, the caused high mortality; however, imidacloprid was less toxic 402
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367 lethal effects of pesticides was higher than the control in to the adults. Despite these two compounds belong to 403
both ages. In the first age, abamectin caused a higher neonicotinoids chemical group, acting on insects’ nervous
U

368 404
369 mortality than thiamethoxam and chlorfenapyr, while the system, the probable cause was the production of metabo- 405
370 mortality caused by all products was similar in the second lites in molecular hydrolysis of thiamethoxam, which may 406
371 age. Similarly as the 48 h evaluation, the mortality of each have intensified the effect on this natural enemy (Simon- 407
372 product was different between 2-h and 12-day residues, Delso et al. 2015). Neonicotinoids are widely used to 408
373 with lower mortality in the second age. control pests in many crops, by spraying, soil application 409
Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator. . .

Cresswell et al. 2012; Ciarlo et al. 2012; Farooqui 2013; 419


Berenbaum and Johnson 2015). Likewise, natural enemies, 420
in particular zoophytophagous predators that feed on sap 421
and other plant resources, are also susceptible to neonico- 422
tinoids (Horowitz and Ishaaya 2004; Torres et al. 2010). 423
The toxicity of these compounds to predatory bugs is 424
corroborated by other studies. Imidacloprid was considered 425
toxic to Podisus maculiventris (Say) (Hemiptera: Pentato- 426
midae) (De Cock et al. 1996) and O. laevigatus (Delbeke 427
et al. 1997). Studebaker and Kring (2003) found that imi- 428
dacloprid was harmful to Orius insidiosus (Say) (Hemi- 429
ptera: Anthocoridae) nymphs in laboratory conditions. In 430
the same context, Prabhaker et al. (2011) observed that 431
thiamethoxan and imidacloprid were toxic to the predator 432
Geocoris punctipes (Say) (Hemiptera: Geocoridae) and O. 433
insidiosus. 434
Abamectin was classified as moderately harmful to 435
nymphs and adults, causing more than 90% mortality on the 436
evaluated insects. This product affects mainly the 437
glutamate-gated chloride channels, which are responsible 438
for several activities on insects, such as locomotion, feeding 439
and sensitive inputs (Wolstenholme 2012). Despite rapid 440
degradation, abamectin has low specificity; therefore, it can 441

F
affect both the pests and natural enemies (Wislocki et al. 442

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1989), which may compromise its use in IPM programs. 443
The deleterious effects of abamectin to natural enemies was 444
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evaluated by other researchers. For example, Kim et al. 445
(2006) reported high toxicity of abamectin to nymphs and 446
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adults of the predator Deraeocoris brevis (Uhler) (Hemi- 447


ptera: Miridae) either by topical application or residual 448
contact. This compound also caused high mortality of M. 449
basicornis nymphs and adults (Passos et al. 2017), O.
D

450
insidiosus nymphs (Rocha et al. 2006) and reduced hatching 451
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of nymphs and their survivorship (Moscardini et al. 2013). 452


Teflubenzuron caused the lowest mortality on E. varians; 453
however, this compound reduced the progeny of females 454
EC

when they were treated as nymphs and it was not considered 455
harmless in any bioassays. According to Ishaaya and Hor- 456
Fig. 1 Cumulative mortality (mean ± SE) of E. varians third instar owitz (1998), insecticides inhibiting chitin synthesis such as 457
nymphs after 24, 48 and 72 h of exposure to two residue ages (2-h and
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12-day) of thiamethoxam, abamectin and chlorfenapyr. Bars in each teflubenzuron act mainly by ingestion, but some compounds 458
group labeled with different lower case letters are significantly dif- can present toxicity by contact and adversely affect the 459
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ferent between treatments, while capital letters show difference fertility of insects. The low toxicity of this insecticide on 460
between residue ages (P < 0.05) adults observed in the present study corroborates the lit-
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461
erature reports, confirming its highest effects on immature 462
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410 and seed treatment (Casida 2018). Moreover, they have a stages of insects (Sun et al. 2015). Angeli et al. (2005) also 463
411 broad spectrum of action and are easily translocated in reported the effect of this compound on the predator O. 464
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412 plants through xylem and phloem (Rortais et al. 2005). laevigatus, and the reduction in fecundity was higher when 465
These characteristics imply in high probability to reach and the predator was contaminated via ingestion. Brown et al.
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413 466
414 cause adverse effects on non-target organisms. Several (2003) found low mortality of adult of O. laevigatus 467
415 deleterious effects were reported when pollinators fed on females when exposed to plants treated with teflubenzuron. 468
416 contaminated pollen and nectar, such as alterations in Similarly, Passos et al. (2017) related that this compound 469
417 longevity, survival rates, learning, memory abilities and the caused low mortality to nymphs and adults of M. basi- 470
418 metabolic processes (Wu et al. 2015; Blacquière et al. 2012; cornis. Despite the highest effect of teflubenzuron on E. 471
D. A. Pérez-Aguilar et al.

472 varians nymphs, this product showed lower effect on adults. Abbott WS (1925) A method of computing the effectiveness of an 522
473 Therefore, the use of this product associated with releases of insecticide. J Econ Entomol 18:265–267 523
Abdollahi M, Ranjbar A, Shadnia S et al. (2004) Pesticides and oxi- 524
474 E. varians adults appears to be a possible strategy in T.
dative stress: a review. Med Sci Monit 10:141–147 525
475 absoluta management. Angeli G, Baldessari M, Maines R et al. (2005) Side-effects of pesticides 526
476 On the other hand, in semifield bioassays the insecticides on the predatory bug Orius laevigatus (Heteroptera: Anthocoridae) 527
477 clorphenapyr, abamectin, and thiamethoxam caused high in the laboratory. Biocontrol Sci Technol 15:745–754 528
Arnó J, Gabarra R (2011) Side effects of selected insecticides on the 529
478 mortality on third instar of E. varians when they were
Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus 530
479 exposed to their residues on the same day that the plants pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest 531
480 were treated. All three compounds evaluated under our Sci 84:513–520 532
481 conditions have translaminar action; therefore, the insects Berenbaum MR, Johnson RM (2015) Xenobiotic detoxification path- 533
ways in honey bees. Curr Opin Insect Sci 10:51–58 534
482 may have been contaminated with residues of pesticides by
Biondi A, Campolo O, Desneux N et al. (2015) Life stage-dependent 535
483 two ways of uptake (ingestion and contact with residues), susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphe- 536
484 due to the zoophytophagus habit of E. varians. When linidae) to two pesticides commonly used in citrus orchards. 537
485 insects have fed on the plant sap, pesticide molecules pre- Chemosphere 128:142–147 538
Biondi A, Desneux N, Siscaro G et al. (2012a) Using organic-certified 539
486 sent in the foliar tissue might have been ingested, resulting
rather than synthetic pesticides may not be safer for biological 540
487 in high mortality on the nymphs. However, when nymphs control agents: Selectivity and side effects of 14 pesticides on the 541
488 were exposed to pesticide residues on plants 12 days after predator Orius laevigatus. Chemosphere 87:803–812 542
489 application the mortality was reduced. The lower mortality Biondi A, Guedes RNC, Wan F-H et al. (2018) Ecology, worldwide 543
spread, and management of the invasive South American tomato 544
490 in the second evaluation date confirmed our expectations,
pinworm, Tuta absoluta: Past, present, and future. Annu Rev 545
491 due to the natural degradation of the compounds in green- Entomol 63:239–258 546
492 house conditions, caused mainly by the incidence of solar Biondi A, Mommaerts V, Smagghe G et al. (2012b) The non-target 547
493 radiation (Yu 2008). Despite the high toxicity in lab and at impact of spinosyns on beneficial arthropods. Pest Manag Sci 548
68:1523–1536 549
494 the first date in greenhouse, all products evaluated showed

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Biondi A, Zappalà L, Stark JD et al. (2013) Do biopesticides affect the 550
495 small persistence of lethal effect to E. varians on tomato demographic traits of a parasitoid wasp and its biocontrol services 551

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496 plants. The results indicate that the use of these pesticides through sublethal effects? PLOS ONE 8:e76548 552
497 can be associated with E. varians releases on tomato crops, Blacquière T, Smagghe G, Van Gestel CA et al. (2012) Neonicotinoids 553
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498 since a period of at least 12 days separate pesticide spraying
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499 and predators’ release.
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Brown AS, Simmonds MSJ, Blaney WM (2003) Influence of a short 556
500 In general, our results suggest that teflubenzuron is exposure to teflubenzuron residues on the predation of thrips by 557
501 compatible with releases of E. varians adults to control T. Iphiseius degenerans (Acari: Phytoseiidae) and Orius laevigatus 558
(Hemiptera: Anthocoridae). Pest Manag Sci 59:1255–1259 559
502 absoluta. However, applications of chlorfenapyr, thia-
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methoxam, abamectin and imidacloprid should be avoided
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503 selectivity to natural enemies: challenges and constraints for 561


504 in integrated pest management programs of T. absoluta research and field recommendation. Ciênc Rural 47:e20160829 562
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505 where the presence of E. varians is desirable; if applications Bueno VHP, Van Lenteren JC, Lins JC et al. (2013) New records of 563
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506 of these pesticides are necessary, the predators’ release
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507 should be delayed after spraying the products. Nevertheless, Calvo FJ, Lorente MJ, Stansly PA et al. (2012) Preplant release of 566
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508 an assessment of these compounds under field conditions is Nesidiocoris tenuis and supplementary tactics for control of Tuta 567
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Appl 143:111–119 569
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510 Acknowledgements D.AP-A received a premaster fellowship from


Palaearctic region to beyond: Tuta absoluta 10 years after 571
511 Consejo Nacional de Ciencia y Tecnología-Mexico. This work was
invading Europe. J Pest Sci 90:787–796 572
financially supported by the Coordinación de la Investigación Cientí-
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