Revista de Ciencias Agrícolas p-ISSN 0120-0135 e-ISSN 2256-2273 Research Article: Agronomy

doi: https://doi.org/10.22267/rcia.1936E.108 Effects of imidacloprid-sodium chloride association on survival and reproduction of the stink bug nigrispinus

Podisus nigrispinus Efectos de la asociación de imidacloprid-cloruro de sodio en la supervivencia y Gabryele Silvareproducción Ramos1, Paula Daianadel chinche de Paulo 2, Pedro F. S. Toledo3, Khalid Haddi4†, Jose Cola Zanuncio5, Eugenio E. Oliveira6

ARTICLE DATA ABSTRACT

Ph.D. Plant Protection Departament. Universidade 1 Pesticide effects on natural enemies in an agroecosystem are of paramount

Estadual de São Paulo, Botucatu, SP, Brasil. importance for integrated pest management programs. Natural enemies can [email protected]. Entomology Departament. Universidade 2 ufv.br be subject to direct and indirect exposure to insecticides and synergistic Federal de Viçosa, Viçosa, MG, Brasil. paula.paulo@ of agricultural crops such as soybean. Here, we evaluated the potential effects MSc. Entomology Departament, Universidade ofmolecules imidacloprid (e.g., sodiumand its chlorideinteraction - NaCl) with which NaCl areas anused enhancer to control on various the survival pests 3 Podisus nigrispinus Federal de Viçosa, Viçosa, MG, Brasil. pedro. 4† [email protected]. Entomology Departament, Universidade and reproductive abilities of the non-target predator (Dallas) (: ). The were exposed to the stink Federal de Lavras, Lavras, MG, Brasil. khalid. bugs control field recommended dose of imidacloprid associated or not with 5 [email protected]. Entomology Departament, Universidade affect the survival of P. nigrispinus the salt at the concentration of 0.5% (w/v). NaCl as a pesticide enhancer did not ufv.br adults after 48 h of exposure (less than 12% Federal de Viçosa, Viçosa, MG, Brasil. zanuncio@ Ph.D. Entomology Departament, Universidade of mortalityP. nigrispinus was includedalways recorded). a decrease However, in the oviposition, the fifth instar showing nymph fewer mortality eggs 6 was almost 50%. The effects of imidacloprid on the reproductive parameters

Federal de Viçosa, Viçosa, MG, Brasil. [email protected] Cite per day. However, the fertility was not affected. The NaCl addition, therefore, : Ramos, G., De Paulo, P., Toledo, P., Haddi, thehad presence no effect of on P. thenigrispinus mortality, demonstrated survival, and compatibility, reproduction however, of the non-targetit requires andK., reproduction Zanuncio, J., of Oliveira, the stink E.bug (2019).Podisus nigrispinus. Effects of furtherpredator. evaluation The use ofto NaClendorse associated the set of to these imidacloprid pest control and strategies.other pesticides in Revistaimidacloprid-sodium de Ciencias Agrícolas. chloride association doi:on survival https://

36(E): 71-81. Keywords: doi.org/10.22267/rcia.1936E.108 selectivity. Asopinae, biological control, ecotoxicology, IPM, pest control, Received: October 10 2019. Accepted: October 20 2019. RESUMEN

Los efectos de los pesticidas sobre los enemigos naturales en un

agroecosistema son de suma importancia para los programas de manejo integrado de plagas. Los enemigos naturales pueden estar sujetos a la exposición directa e indirecta de insecticidas y moléculas sinérgicas (por ejemplo, cloruro de sodio - NaCl) que se utilizan para controlar diversas deplagas la supervivencia de cultivos agrícolas y las capacidades como la soja. reproductivas Aquí, evaluamos del depredador los posibles no efectos delPodisus imidacloprid nigrispinus y (Dallas) su interacción (Hemiptera: con NaCl Pentatomidae como un Los potenciador insectos fueron expuestos a una tasa de campo de imidacloprid, recomendado para objetivo

controlar los chinches en campos de soya. La solución P. nigrispinus de imidacloprid después fue mezclada (o no) con NaCl (0.5%, w/v). El NaCl como potenciador de pesticidas no afectó la supervivencia de los adultos de de 48 h de exposición (siempre se registró menos del 12% de mortalidad). UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 72 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus.

parámetros reproductivos de P. nigrispinus Sin embargo, la mortalidad de la ninfa del quinto estadio fue casi del 50%. Los efectos de imidacloprid sobre los incluyeron una disminución en la oviposición, mostrando menos huevos por día. Sin embargo, la fertilidad no se vio afectada. La adición de NaCl, por lo tanto, no tuvo efecto sobre la mortalidad, supervivencia y reproducción del depredador no objetivo. El uso de NaCl asociado a imidacloprid y otros pesticidas en presencia de P. nigrispinus demostró compatibilidad, sin embargo, requiere una evaluación adicional para respaldar el conjunto de estas estrategias de control de plagas. Palabras clave:

Asopinae, control biológico, ecotoxicología, MIP, control de plagas, selectividad.

INTRODUCTION insecticide solutions is, supposedly, believed to decrease the quantities of pesticide by half Glycine max L., presents Panizzi et al. theThe productivity soybean, of these plants is severely (50%) without losing efficiency (Corso, 1990; great economic importance in Brazil and , 2007; Ávila and Grigolli, 2014). insects, besides decreasing productivity, phagostimulant or arrestant molecule, which substantiallyaffected by raise the cost pest of attacks.production These due increasesIt is believed the insect that contact NaCl (exposure acts period) like a to pest management strategies which are of with the pesticide solution or dry residues et al. Peterson et al. unquestioned need (Ávila and Grigolli, 2014; (Corso, 1990; Sosa-Gómez , 1993; Niva Among other, 2018).insect pests, the herbivory and Panizzi, 1996; Corso and Gazzoni, 1998). byThe the existence presence of salt of neuroreceptorsaction on the pentatomid sensitive which includes over three of stink tostink low bugs concentrations nervous system of sodium was confirmed chloride, attacks delivered by a “stink bug complex”, causing a simultaneous attraction (Gr5a bugs, is considered one of the major barrierset al., behavior (Yarmolinsky et al. to the development of soybean crop fields in receptors) and deterrence (Gr66a receptors) instance,Brazil and the other Neotropical countries stink (Da bug, Graça Euchistus A couple of recent works, 2009).tried to better heros2016). (Fabr.) The management (Hemiptera: of suchPentatomidae) pests, for elucidate the actions of imidacloprid (Haddi et heavily relies on the use of synthetic al. et al. pesticides, which includes, organophosphates, effects of NaCl added to some pesticides are pyrethroids, organochlorides (endosulfan) not, 2016; fully Santosexplained ,and 2016), still but need the synergicfurther and neonicotinoids (Panizzi et al. investigations that address the reasons et al. underlying the aforementioned synergism as , 2012; well as the reasons why it occurs only with Tuelher , 2018). some pesticides. et al., The neonicotinoids,et al. acting as agonists of acetylcholine receptors (Buckingham pest management programs in soybean 1997; Nauen , 2001), are among the The use of biological control and integratedAnticarsia most used pesticides in soybean fieldset andal., gemmatalis are frequently usedet al. by Brazilian farmers Noctuidae),fields, especially and somefor the other control stink of bugs have due to their high efficiency (Pazini also had favorable (Hübner, results 1818) (Ramiro (Lepidoptera: et al., 2019; Castellanos , 2019). Furthermore, Podisus a common practice in Brazilian soybean nigrispinus, Hemiptera: Pentatomidae, fields consisting of adding sodium chloride 1986). Predatory stink bugs, e.g., (NaCl) at the concentration of 0.5% (w/v) to UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus. 73 naturally occur in the Neotropical region (in considered very important natural enemies cage. The stem of the branches was kept inside ofmany defoliator crop fields, caterpillars including (Pires soybean) et al. and are colonya glass flaskwas kept(15 mLunder of volume controlled capacity) conditions filled Holtz et al. with water to keep them± °C), hydrated. photoperiod The stock (12h , 2006, scotophase), and humidity (70 ± , 2019). etof al.temperature (25 2 of costs ecological services aiding in the 10%) (Lemos managementThese predatory of soybean insects pests delivery and their have freethe Bioassays, 2003). potential to be introduced to enhance the power of other pest control strategies, in Acute toxicity against the predatory stink cases of augmentative biological control uses bug Podisus nigrispinus. Newly emerged (Desneux et al. et al et al. et al. et al., hours) were exposed to dry residues of the , 2007; Batalha ., 2012; He fifth instar nymphs and adult females (< 72 , 2012; Naranjo , 2015; Bueno used conventional pesticides and their imidacloprid to control E. heros in soybean enhancers2017). However, (e.g., NaCl) the impactshave been of completely commonly recommended field rate (4.2µg a.i./cm²) of neglected for predatory stink bugs. Hence, it is of extreme importance to study the potential addedfields or (MAPA, not with 2018) NaCl was with used or as without the control. the selectivity/compatibility of these compounds addition of NaCl 0.5% (w/v). Distilled water to natural enemies. with glass surface impregnated with dried Insecticide exposure was achieved by contact potential effects including side effects on the residues. Briefly, 2mL of insecticide solution reproductiveThus, this study abilities aimed of tothe investigate neonicotinoid the Paulicéiof distilled water were applied to 250mL imidacloprid associated to NaCl which transparent glass jars (EME Equipment, is highly recommended for controlling a, SP, Brazil), which were maintained the Neotropical stink bug E. heros on the under rotation until dry using a heavy‐duty predatory stink bug P. nigrispinus. rotator (Roto‐Torque model 7637, ColeParmer, portionVernon Hills,of each IL, USA)container to coat was the coated inner wallswith of the jars with insecticide residue. The upper MATERIAL AND METHODS nymphsTeflon PTFE or adult (DuPont, females, Wilmington, were set insideDE, USA) the Insect rearing to prevent insects from escaping. Ten insects,

Podisus nigrispinus. Eggs of Podisus didglass not flasks move and orthe cannot exposure walk period a distance was 48 nigrispinus correspondinghours. Insects to were double considered the size of dead their when own water (soaked were cotton field-collected wool) andto provide kept in humidity.Petri dishes After (9cm egg diameter) hatching, with immature distilled body for one minute.± The°C experimentsrelative humidity were kept± under laboratory-controlled conditions made by wood (frame) and veil cloth of temperature 25 2 stages were transferred to cages (30x15cm)Tenebrio each60 P. 10% nigrispinus and L:D stage photoperiod and treatment. of 14:10h. molitor Was performed at least nine replicates for Additionally,(coverage). TheyEucalyptus were fedspp. with leaves were provided L. by(Coleoptera: setting a small Tenebrionidae) branch inside pupae. the hour exposure were kept individualized in The survivor insects that came from the 48-

UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 74 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus.

and variance homogeneity were not met, the withPetri pupaedishes of (diameter: T. molitor, Eucalyptus90 mm) bottom-side spp. leaves covered with filter paper. Insects were fed mortality was subjected to Kruskal-Wallis method)test ate 5% and probability. the reproductive Survival analysisparameters was (7cm stem containing three or four leaves) datasubjected (daily toegg Kaplan-Meier and nymphs numbers) test (LogRank were and distilled water (soaked cotton wool). The ±experiments were kept under± laboratory- controlled conditions of temperature 25 respectively submitted to Tukey and Kruskall- replicates 2°C relative each humidity insect was 60 considered 10% and one L:D USA).Wallis tests (P< 0.05) using SigmaPlot version replicate.photoperiod of 14:10h. Was performed 88 12.5 software (Systat Software, San Jose, CA,

Sublethal effects on the reproduction RESULTS AND DISCUSSION of Podisus nigrispinus females. Newly emerged adults of P. nigrispinus Toxicity to the fifth instar of Podisus were exposed individually to dry residues nigrispinus. (24h) nymphs of P. nigrispinus µg a.i./cm E. heros (which is equivalentThe exposure to the ofrecommended fifth instar2 of the recommended field rate (4.2µg a.i./ E. heros to) with 4.2 or without withoutcm²) of the imidacloprid addition of to sodium control chloride at the addition of NaCl differed from the control in soybean fields (MAPA, 2018) with or field rate to control group (H P earlier. Distilled water was added with occasioned by the neonicotinoid imidacloprid sodiumthe concentration chloride or of not 0.5% as control(m/v) as treatments. described (associated= 21.35; or not

UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus. 75

Figure 1 (A) and adult females (B) of Podisus nigrispinus imidacloprid. Mortality (associated of fifth or not instar to NaCl). nymphs after 48-hour of exposure to 4.2 µg a.i./cm² of

Survival of exposed Podisus nigrispinus. of P. nigrispinus adults were 20.7 ± 2.43; Survival of P. nigrispinus adults did not 20.3 ± 2.24; 16.1 ± 1.4 and 14.9 ± exposed insects (Log Rank = P= imidacloprid, imidacloprid with 0.98the dayssalt differ between unexposed and imidacloprid- addition,in the treatments only water using and thewater field with dose salt of 7.5; 0.06). The median survival time ranged from 15.1 to 20.7 days. The survival averages (0.5% w/v), respectively (Figure 2).

Figure 2. Survival curves of Podisus nigrispinus

of imidacloprid (associated or not to NaCl) using the adults after 48 hours of exposure to 4.2 µg a.i./cm²

rank test (Log Rank df = P = Kaplan-Meier method and compared using the log- =3 7.51; 0.057). UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 76 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus.

Sublethal effects on the reproduction of B) fertility of this natural enemy (H Podisus nigrispinus females. Fecundity P and fertility of P. nigrispinus females were caused(Figure by3 the pesticide exposure affected the similar between treatments without total= 21.4; (Figure < 0.001). 4A) andThis dailyreduction nymph in fecundityhatching (Figure 4B) which differed from the control contrary, imidacloprid associated or not to with water (H P insecticide (Figures 3 and 4).A) and On daily the plus salt (H P = 9.80; = 0.014) and water NaCl reduced the total (Figure 3 = 9.80; = 0.016).

Figure 3. Fertility of adult females of Podisus nigrispinus (A) Fertility graphic based on the total number of eggs and (B) Fertility graphic after of 48-hour daily number exposure of eggsto 4.2 hatched. µg i.a./cm² of imidacloprid (associated or not to NaCl).

Figure 4. Fecundity of Podisus nigrispinus (A) Fecundity graphic (B) adults after 48 hours of exposure to number4.2 µg i.a./cm² hatched. of imidacloprid (associated or not to NaCl). of total nymphs’ number hatched and Fecundity graphic of daily nymphs’

UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus. 77

Studying the potential impacts of (Corso et al. conventional pesticides and their synergists of a neuronal response in the expression of Gr5a receptors, 1990). stimulated These effectson the may presence result unquestioned need. Although neonicotinoid insecticides(e.g., NaCl) againsthave been beneficial thriving organisms on the market is of results in aversion to NaCl (Yarmolinsky et due to their power to control insect pests, they al.of low NaCl concentrations and Gr66a which have received attention regarding their side P. nigrispinus due to its different life history , 2009). Such response may be absent in bees and natural enemies and it becomes a of action, as well as the presence of tarsal moreeffects pessimistic on non-target scenario organisms in the e.g., presence pollinating of sensillatraits the that differential may alter confirmation the toxicodynamic of its site of pesticide enhancers. the NaCl (Focks et al.

, 2018). that imidacloprid solutions (regardless of affect the nutrient uptake, disaggregation, In the present study, we have demonstrated digestiveToxic effects physiology caused by and imidacloprid reproductive may instar nymphs of the predatory stink bug P. nigrispinussalt addition). On increased the other hand,the mortality those pesticide of fifth et al. solutions neither caused mortality nor etabilities al. and behavior et of al. the non-target affected the survival of P. nigrispinus adults. neonicotinoidspredator (Magalhães had been, 2002; reported Malaquias as A higher survival of P. nigrispinus adults molecules, 2014; that Martínezdid not affect the, 2019).oviposition The compared to its nymphal stages fourth and and egg hatch of treated female adults of Podisus sp. and showing lower mortality and as imidacloprid, pyriproxyfen and neem oil survival impacts compared with to residual fifth instars after exposure to pesticides such toxicity of pyrethroid molecules (De Cock et et al. al. has been demonstrated elsewhere (Zanuncio et al. lower, concentration 2016). The increasedof detoxifying susceptibility enzymes , 1996; Tillman and Mullinix, 2004; Torres (esterases)of insect immatureas well as the stages cuticle may composition reflect a eggsand Ruberson,was not affected 2004; Pereira by the imidacloprid, 2005). (Guedes et al. et al. withThese or results without suggest salt but that the the fertility viability of of thisthe Hence, our results reinforced that immature predator was reduced in agreement with stages of this ,predatory 1992; Zanuncio stink bug are, 2001). more results for pesticides reducing mature susceptible to pesticides . oocytes and increasing the maturation period of P. nigrispinus (Reis et al. and NaCl as an enhancer allowed the control , 2018). ofThe Piezodorus mixture of guildinii thiamethoxan,, Nezara cypermethrin, viridula and reduction in the amount of insecticide E. heros species for longer periods (up to appliedThe use to ofsoybean salt ascrops, a synergistreducing the favors farms a et al. synergistic agent in insecticide solutions due as well as causing a lower environmental to15 thedays) preference (Ramiro of pest, 2005). insects The forNaCl areas is a expenditure on inputs (i.e., increasing profit), treated with low NaCl concentrations (Corso enhancer (i.e., NaCl) did not impact any et al. ofimpact. the parameters Interestingly, evaluated the addition here offor theP. nigrispinus. insectand Gazzoni, pests through 1998; Marcominian arresting effect, 2016).which makesThis synergist them morecauses dynamicshifts on theon behaviorthe plant, of imidacloprid,The but fecunditynot to the dataaddition show of salt. that increasing insect exposure to insecticides the non-target predator is susceptible to

The treatments that contained the field dose UNIVERSIDAD DE NARIÑO Rev. Cienc. Agr. June - December 2019 Volume 36(E): 71 - 81 78 Ramos et al-. Imidacloprid-sodium chloride association on survival and reproduction Podisus nigrispinus. of this insecticide presented lower number of Conflict of interest: nymphs compared to that with water or water with salt. Even though imidacloprid increases The authors declare that the mortality and impacts the fertility and they have no conflict of interest. fecundity of P. nigrispinus, the addition of BIBLIOGRAPHIC REFERENCES NaCl which supposedly increase the strength of pesticides against stink bug pests did not Ávila, C. impact the evaluated parameters. Sublethal doses of imidacloprid showed effects on the B. & Grigolli,Fundação J.F.J. (2014)MS. Recovered Pragas de from soja e seu controle. Tecnologia e Produção: Soja medium intestine , affecting of P. nigrispinus 2013/2014. severally the digestion capacity consequently http://www.fundacaoms.org.br/tecnologia- the predatory potential (Martínez et al., producao-soja-2013-2014. Selectivity Batalha,of insecticides V.C., Zanuncio, to Podisus J.C., Picanco,nigrispinus M. 2019). CONCLUSIONS (Heteroptera:& Guedes, R.N.C.Pentatornidae) (2012). and its prey Spodoptera frugiperda (Lepidoptera: Noctuidae). Ceiba, 38

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