Abstract
The control of defoliating caterpillars in forestry includes the use of insecticides and releases of the predatory bug Podisus nigrispinus, but some compounds may affect non-target natural enemies, which need evaluation of risk assessment. This research investigates the survival, preference, and prey consumption of P. nigrispinus adults fed with prey treated with the lethal concentration (LC50) of Bacillus thuringiensis (Bt), permethrin, tebufenozide, and thiamethoxam. Moreover, midgut histopathology of P. nigrispinus fed with preys treated with LC50 of each insecticide was investigated. The insecticides Bt, permethrin, and thiamethoxam reduce the survival and the prey consumption in P. nigrispinus fed with preys contaminate with these chemicals. However, the four tested insecticides, including tebufenozide, cause histological changes such as irregular epithelial architecture, cytoplasm vacuolization, and release of cell fragments in the midgut lumen of P. nigrispinus. The sublethal effects of Bt, permethrin, tebufenozide, and thiamethoxam to the natural enemy suggest that they should be better evaluated to be used together with P. nigrispinus for integrated pest management in forestry.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article (and its Supplementary information files).
References
Arthidoro de Castro MB, Martinez LC, Cossolin JFS, Serra RS, Serrão JE (2020) Cytotoxic effects on the midgut, hypopharyngeal glands and brain of Apis mellifera honey bee workers exposed to chronic concentrations of lambda-cyhalothrin. Chemosphere 248:126075. https://doi.org/10.1016/j.chemosphere.2020.126075
Bacci L, Picanço MC, Barros EC, Rosado JF, Silva GA, Silva VF, Silva NR (2009) Physiological selectivity of insecticides to wasps (Hymenoptera: Vespidae) preying on the diamondback moth. Sociobiology 53:151–167
Backus EA (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: a taxonomic overview. J Insect Physiol 34:151–165. https://doi.org/10.1016/0022-1910(88)90045-5
Camargo C, Hunt TE, Giesler LJ, Siegfried BD (2017) Thiamethoxam toxicity and effects on consumption behavior in Orius insidiosus (Hemiptera: Anthocoridae). Environ Entomol 46:693–699. https://doi.org/10.1093/ee/nvx050
Carneiro LS, Martínez LC, Gonçalves WG, Santana LM, Serrão JE (2020) The fungicide iprodione affects midgut cells of non-target honey bee Apis mellifera workers. Ecotoxicol Environ Saf 189:10999. https://doi.org/10.1016/j.ecoenv.2019.109991
Castro BM, Martínez LC, Barbosa SG, Serrão JE, Wilcken C, Soares MA, Silva AA, Carvalho AG, Zanuncio JC (2019) Toxicity and cytopathology mediated by Bacillus thuringiensis in the midgut of Anticarsia gemmatalis (Lepidoptera: Noctuidae). Sci Rep 9:6667. https://doi.org/10.1038/s41598-019-43074-0
Castro BMC, Martínez L, Plata-Rueda A, Soares MA, Wilcken C, Zanuncio AJV, Fiaz M, Zanuncio JC, Serrão JE (2021) Exposure to chlorantraniliprole reduces locomotion, respiration, and causes histological changes in the midgut of velvetbean caterpillar Anticarsia gemmatalis (Lepidoptera: Noctuidae). Chemosphere 263:128008. https://doi.org/10.1016/j.chemosphere.2020.128008
Cordeiro EMG, Corrêa AS, Venzon M, Guedes RNC (2010) Insecticide survival and behavioral avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81:1352–1357. https://doi.org/10.1016/j.chemosphere.2010.08.021
Cossolin JFS, Pereira MJB, Martínez LC, Turchen LM, Fiaz M, Bozdoğan H, Serrão JE (2019) Cytotoxicity of Piper aduncum (Piperaceae) essential oil in brown stink bug Euschistus heros (Heteroptera: Pentatomidae). Ecotoxicology 28:763–770. https://doi.org/10.1007/s10646-019-02072-8
De Bortoli SA, Otuk AK, Vacari AM, Martins MIEG, Volpe HLX (2011) Comparative biology and production costs of Podisus nigrispinus (Hemiptera: Pentatomidae) when fed different types of prey. Biol Control 58:127–132. https://doi.org/10.1016/j.biocontrol.2011.04.011
De Castro AA, Corrêa AS, Legaspi JC, Guedes RNC, Serrão JE, Zanuncio JC (2013) Survival and behavior of the insecticide-exposed predators Podisus nigrispinus and Supputius cincticeps (Heteroptera: Pentatomidae). Chemosphere 93:1043–1050. https://doi.org/10.1016/j.chemosphere.2013.05.075
De Castro AA, Poderoso JCM, Ribeiro R, Legaspi JC, Serrão JE, Zanuncio JC (2015) Demographic parameters of the insecticide-exposed predator Podisus nigrispinus: implications for IPM. BioControl 60:231–239. https://doi.org/10.1007/s10526-014-9639-y
Denecke S, Swers L, Douris V, Vontas J (2018) How do oral insecticidal compounds cross the insect midgut epithelium? Insect Biochem Mol Biol 103:22–35. https://doi.org/10.1016/j.ibmb.2018.10.005
Dutra CC, Koch RL, Burkness EC, Meissle M, Romeis J, Hutchison WD, Fernandes MG (2012) Harmonia axyridis (Coleoptera: Coccinellidae) exhibits no preference between Bt and non-Bt maize fed Spodoptera frugiperda (Lepidoptera: Noctuidae). PLoS One 7:e44867. https://doi.org/10.1371/journal.pone.0044867
Dutton A, Klein H, Romeis J, Bigler F (2003) Prey-mediated effects of Bacillus thuringiensis spray on the predator Chrysoperla carnea in maize. Biol Control 26:209–215. https://doi.org/10.1016/S1049-9644(02)00127-5
Ferreira JAM, Zanuncio JC, Torres JB, Molina-Rugama AJ (2008) Predatory behaviour of Podisus nigrispinus (Heteroptera: Pentatomidae) on different densities of Anticarsia gemmatalis (Lepidoptera: Noctuidae) larvae. Biocontrol Sci Tech 18:711–719. https://doi.org/10.1080/09583150802271220
Fialho MCQ, Terra WR, Moreira NR, Zanuncio JC, Serrão JE (2013) Ultrastructure and immunolocalization of digestive enzymes in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae). Arthropod Struct Dev 42:277–285. https://doi.org/10.1016/j.asd.2013.03.002
Fiaz M, Martínez LC, Plata-Rueda A, Gonçalves WG, Shareef M, Zanuncio JC, Serrão JE (2018) Toxicological and morphological effects of tebufenozide on Anticarsia gemmatalis (Lepidoptera: Noctuidae) larvae. Chemosphere 212:237–345. https://doi.org/10.1016/j.chemosphere.2018.08.088
Godoy MS, Carvalho GA, Moraes JC, Cosme LV, Goussain MM, Carvalho CF, Morais AA (2004) Seletividade de seis inseticidas utilizados em citros a pupas e adultos de Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Neotrop Entomol 33:359–364. https://doi.org/10.1590/S1519-566X2004000300014
Lemes P, Zanuncio JC, Serrão JE, Lawson SA (2017) Forest Stewardship Council (FSC) pesticide policy and integrated pest management in certified tropical plantations. Environ Sci Pollut R 24:1283–1295. https://doi.org/10.1007/s11356-016-7729-3
Lindenmayer DB, Margules CR, Botkin DB (2000) Indicators of biodiversity for ecologically sustainable forest management. Conserv Biol 14:941–950. https://doi.org/10.1046/j.1523-1739.2000.98533.x
Lopes MP, Fernandes KM, Tomé HVV, Gonçalves WG, Miranda FR, Serrão JE, Martins GF (2018) Spinosad-mediated effects on the walking ability, midgut, and Malpighian tubules of Africanized honey bee workers. Pest Manag Sci 74:1311–1318. https://doi.org/10.1002/ps.4815
Malaquias JB, Omoto C, Ramalho FS, Wesley WAC, Silveira RF (2014) Bt cotton and the predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) in the management of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) resistance to lambda-cyhalothrin. J Pest Sci 88:57–63. https://doi.org/10.1007/s10340-014-0585-3
Martínez LC, Fialho MDCQ, Zanuncio JC, Serrão JE (2014) Ultrastructure and cytochemistry of salivary glands of the predator Podisus nigrispinus (Hemiptera: Pentatomidae). Protoplasma 251:535–543. https://doi.org/10.1007/s00709-013-0549-0
Martínez LC, Fialho MCQ, Barbosa LCA, Oliveira LL, Zanuncio JC, Serrão JE (2016) Stink bug predator kill prey with salivary non-proteinaceous compounds. Insect Biochem Mol Biol 68:71–78. https://doi.org/10.1016/j.ibmb.2015.11.006
Martínez LC, Plata-Rueda A, da Silva NG, Gonçalves WG, Zanuncio JC, Bozdogan H, Serrão JE (2018) Permethrin induces histological and cytological changes in the midgut of the predatory bug, Podisus nigrispinus. Chemosphere 212:629–637. https://doi.org/10.1016/j.chemosphere.2018.08.134
Martínez LC, Plata-Rueda A, Rodríguez-Dimaté FA, Campos JM, Santos Júnior V, Rolim GDS, Fernandes FL, Silva WM, Wilcken CF, Zanuncio JC, Serrão JE (2019a) Exposure to insecticides reduces populations of Rhynchophorus palmarum in oil palm plantations with Bud Rot disease. Insects 10(4):111. https://doi.org/10.3390/insects10040111
Martínez LC, Plata-Rueda A, Gonçalves WG, Freire AFPA, Zanuncio JC, Bozdoğan H, Serrão JE (2019b) Toxicity and cytotoxicity of the insecticide imidacloprid in the midgut of the predatory bug, Podisus nigrispinus. Ecotox Environ Safe 167:69–75. https://doi.org/10.1016/j.ecoenv.2018.09.124
Martinou AF, Seraphides N, Stavrinides MC (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus. Chemosphere 96:167–173. https://doi.org/10.1016/j.chemosphere.2013.10.024
Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580. https://doi.org/10.1016/S0165-6147(00)01820-4
Medeiros RS, Ramalho FS, Lemos WP, Zanuncio JC (2000) Age-dependent fecundity and life-fertility tables for Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). J Appl Entomol 124:319–324. https://doi.org/10.1046/j.1439-0418.2000.00482.x
Meier M, Hilbeck A (2001) Influence of transgenic Bacillus thuringiensis corn-fed prey on prey preference of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Basic Appl Ecol 2:35–44. https://doi.org/10.1078/1439-1791-00034
Moser SE, Obrycki JJ (2009) Non-target effects of neonicotinoid seed treatments; mortality of coccinellid larvae related to zoophytophagy. Biol Control 51:487–492. https://doi.org/10.1016/j.biocontrol.2009.09.001
Nadel H, Johnson MW, Gerik M, Daane KM (2007) Ingestion of spinosad bait GF-120 and resulting impact on adult Chrysoperla carnea. Biocontrol Sci Tech 17:995–1008. https://doi.org/10.1080/09583150701618216
Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M (2003) Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic Biochem Physiol 76:55–69. https://doi.org/10.1016/S0048-3575(03)00065-8
Ono ÉK, Zanardi ZO, Santos KFA, Yamamoto PT (2017) Susceptibility of Ceraeochrysa cubana larvae and adults to six insect growth-regulator insecticides. Chemosphere 168:49–57. https://doi.org/10.1016/j.chemosphere.2016.10.061
Pérez-Aguilar DA, Soares MA, Passos LC, Martínez AM, Pineda S, Carvalho GA (2018) Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ecotoxicology 27:719–728. https://doi.org/10.1007/s10646-018-1954-0
Plata-Rueda A, Quintero HA, Serrão JE, Martínez LC (2020a) Insecticidal activity of Bacillus thuringiensis strains on the nettle caterpillar, Euprosterna elaeasa (Lepidoptera: Limacodidae). Insects 11:310. https://doi.org/10.3390/insects11050310
Plata-Rueda A, Menezes CHM, Cunha WS, Alvarenga TM, Barbosa BF, Zanuncio JC, Martínez LC, Serrão JE (2020b) Side-effects caused by chlorpyrifos in the velvetbean caterpillar Anticarsia gemmatalis (Lepidoptera: Noctuidae). Chemosphere 259:127530. https://doi.org/10.1016/j.chemosphere.2020.127530
Rametsteiner E, Simula M (2003) Forest certification—an instrument to promote sustainable forest management? J Environ Manag 67:87–98. https://doi.org/10.1016/S0301-4797(02)00191-3
Riddick EW, Barbosa P (1998) Impact of Cry3A-intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and pollen on consumption, development, and fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae). Ann Entomol Soc Am 91:303–307. https://doi.org/10.1093/aesa/91.3.303
Rolim GS, Plata-Rueda A, Martínez LC, Ribeiro GT, Serrão JE, Zanuncio JC (2020) Side effects of Bacillus thuringiensis on the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Ecotoxicol Environ Saf 189:109978
Santos-Junior VC, Martinez LC, Plata-Rueda A, Fernandes FL, Tavares WS, Zanuncio JC, Serrão JE (2020) Histopathological and cytotoxic changes induced by spinosad on midgut cells of the non-target predator Podisus nigrispinus Dallas (Heteroptera: Pentatomidae). Chemosphere 238:124585. https://doi.org/10.1016/j.chemosphere.2019.124585
Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect–plant biology. Oxford University Press, Oxford
Serra RS, Cossolin JFS, Resende MTCS, Arthidoro de Castro M, Oliveira AH, Martínez LC, Serrão JE (2021) Spiromesifen induces histopathological and cytotoxic changes in the midgut of the honeybee Apis mellifera (Hymenoptera: Apidae). Chemosphere 270:129439. https://doi.org/10.1016/j.chemosphere.2020.129339
Silva WM, Martínez LC, Plata-Rueda A, Serrão JE, Zanuncio JC (2020) Respiration, predatory behavior and prey consumption by Podisus nigrispinus (Heteroptera: Pentatomidae) nymphs exposed to some insecticides. Chemosphere 261:127720. https://doi.org/10.1016/j.chemosphere.2020.127720
Skelhorn J, Rowe C (2007) Predators’ toxin burdens influence their strategic decisions to eat toxic prey. Curr Biol 17:1479–1483. https://doi.org/10.1016/j.cub.2007.07.064
Soderlund DM (2010) State-dependent modification of voltage-gated sodium channels by pyrethroids. Pestic Biochem Physiol 97:78–86. https://doi.org/10.1016/j.pestbp.2009.06.010
Stefanini M, De Martino C, Zamboni L (1967) Fixation of ejaculated spermatozoa for electron microscopy. Nature 216:173–174. https://doi.org/10.1038/216173a0
Sun X, Zhou W, Liu H, Zhang A, Ai CR, Zhou SS, Zhou CX, Wang MQ (2013) Transgenic Bt rice does not challenge host preference of the target pest of rice leaffolder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). PLoS One 8:e79032. https://doi.org/10.1371/journal.pone.0079032
Tadei R, Menezes Oliveira VB, Silva Zacarin ECM (2020) Silent effect on the fungicide pyrachlstrobin on the larval exposure of the non-target organism Africanized Apis mellifera and its interaction with the pathogen Nosema ceranae in adulthood. Environ Pollut 267:115622. https://doi.org/10.1016/j.envepol.2020.115622
Teixeira AD, Fialho MCQ, Zanuncio JC, Ramalho FS, Serrão JE (2013) Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development. Arthropod Struct Dev 42:237–246. https://doi.org/10.1016/j.asd.2013.02.004
Terra WR, Ferreira CL (2020) Evolutionary trends of digestion and absorption in the major insect orders. Arthropod Struc Dev 56:100931. https://doi.org/10.1016/j.asd.2020.100931
Torres JB, Ruberson JR (2008) Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans. Transgenic Res 17:345–354. https://doi.org/10.1007/s11248-007-9109-8
Zanuncio JC, Lemes PG, Antunes LR, Maia JLS, Mendes JEP, Tanganelli KM, Salvador JF, Serrão JE (2016a) The impact of the Forest Stewardship Council (FSC) pesticide policy on the management of leaf-cutting ants and termites in certified forests in Brazil. Ann For Sci 73:205–214. https://doi.org/10.1007/s13595-016-0548-3
Zanuncio JC, Mourão SA, Martínez LC, Wilken CF, Ramalho FS, Plata-Rueda A, Soares MA, Serrão JE (2016b) Toxic effects of the neem oil (Azadirachta indica) formulation on the stink bug predator, Podisus nigrispinus (Heteroptera: Pentatomidae). Sci Rep 6:30261. https://doi.org/10.1038/srep30261
Funding
To the Brazilian agencies “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES), “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG), and the “Programa Cooperativo sobre Proteção Florestal” (PROTEF) to “Instituto de Pesquisas e Estudos Florestais” (IPEF) for scholarships and financial support.
Author information
Authors and Affiliations
Contributions
Wiane Silva, Luis Martínez, and Angelica Plata-Rueda: conceptualization, methodology, and analysis. Wiane Silva: data curation and writing - original draft. Luis Martínez: sampling and software. Luis Martínez, José Serrão, and José Zanuncio: supervision and writing-reviewing and editing.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Giovanni Benelli
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Silva, W.M., Martínez, L.C., Plata-Rueda, A. et al. Exposure to insecticides causes effects on survival, prey consumption, and histological changes in the midgut of the predatory bug, Podisus nigrispinus (Hemiptera: Pentatomidae). Environ Sci Pollut Res 28, 57449–57458 (2021). https://doi.org/10.1007/s11356-021-14589-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14589-9