Lethal and sublethal effects of insecticides on Bathycoelia distincta (Heteroptera: Pentatomidae)


  • Dr Elisa Pal 1Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa 2African Centre of Chemical Ecology, Innovation Africa Campus, University of Pretoria, Pretoria, South Africa https://orcid.org/0000-0002-5799-3440
  • Prof Jeremy D. Allison 1Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa 2African Centre of Chemical Ecology, Innovation Africa Campus, University of Pretoria, Pretoria, South Africa 3Natural Resources Canada-Canadian Forest Service, Great Lakes Forestry Centre, Sault Ste Marie, Canada https://orcid.org/0000-0002-0765-3149
  • Prof Brett P. Hurley 1Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa 2African Centre of Chemical Ecology, Innovation Africa Campus, University of Pretoria, Pretoria, South Africa https://orcid.org/0000-0002-8702-5547
  • Prof Bernard Slippers 2African Centre of Chemical Ecology, Innovation Africa Campus, University of Pretoria, Pretoria, South Africa & 4Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa https://orcid.org/0000-0003-1491-3858
  • Gerda Fourie 2African Centre of Chemical Ecology, Innovation Africa Campus, University of Pretoria, Pretoria, South Africa & 4Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa




stink bug, toxicity, pyrethroids, macadamia


Bathycoelia distincta is one of the most dominant stink bug pests associated with macadamia orchards in South Africa. Understanding the toxicity and sublethal effects of insecticides on this pest is essential for its effective management. This study tested four commercial insecticide formulations, consisting of one organophosphate (acephate) and three pyrethroids (lambda-cyhalothrin, beta-cyfluthrin and tau-fluvalinate). The toxicity of these insecticides and their behavioural effects on mobility were assessed. The sublethal effects of lambda-cyhalothrin on the biological parameters of parent B. distincta (F0) and offspring generations (F1) were also determined by treating B. distincta adults with sublethal concentrations (LC10 and LC30). In toxicity bioassays, acephate was more toxic to B. distincta than lambda-cyhalothrin, beta-cyfluthrin and tau-fluvalinate. Behavioural changes were only observed in bugs exposed to pyrethroids, resulting in an increase in the distance walked and decrease of angular velocity. In the F0 generation, LC30 reduced the fecundity whereas the LC10 and LC30 accelerated development of the F1 generation. These results suggest that pyrethroids may enhance the dispersal of this pest and stimulate the growth of offspring populations. Further experiments should be conducted to confirm these results and understand the mechanism of action of pyrethroids on B. distincta.


Download data is not yet available.


Metrics Loading ...


Abbott W. 1925. A method of computing the effectiveness of an insecticide Journal of Economic Entomology. 18(2):265–267.


Bansal R, Michel A. 2018. Expansion of cytochrome P450 and cathepsin genes in the generalist herbivore brown marmorated stink bug. BMC Genomics. 19(1):60. https://doi.org/10.1186/s12864-017-4281-6.

Bao H, Liu S, Gu J, Wang X, Liang X, Liu Z. 2009. Sublethal effects of four insecticides on the reproduction and wing formation of brown planthopper, Nilaparvata lugens. Pest Management Science. 65(2):170–174. https://doi.org/10.1002/ps.1664.

Blackman B, Lanka S, Hummel N, Way M, Stout M. 2015. Comparison of the effects of neonicotinoids and pyrethroids against Oebalus pugnax (Hemiptera: Pentatomidae) in rice. Florida Entomologist. 98(1):18–26. https://doi.org/10.1653/024.098.0104.

Boff JS, Reis AC, Patricia DSG, Pretto VE, Garlet CG, Melo AA, Bernardi O. 2022. The effect of synergistic compounds on the susceptibility of Euschistus heros (Hemiptera: Pentatomidae) and Chrysodeixis includens (Lepidoptera: Noctuidae) to pyrethroids. Environmental Entomology. 51(2):421–429. https://doi.org/10.1093/ee/nvac005.

Bruwer IJ, Giliomee JH, Pringle KL. 2021. The relationship between proboscis length and the ability of certain Heteroptera to damage macadamia kernels. African Entomology. 29(1):112–124. https://doi.org/10.4001/003.029.0112.

Burrows HD, Canle LM, Santaballa JA, Steenken S. 2002. Reaction pathways and mechanisms of photodegradation of pesticides. Journal of Photochemistry and Photobiology B. 67(2):71–108. https://doi.org/10.1016/S1011-1344(02)00277-4.

Cira TM, Burkness EC, Koch RL, Hutchison WD. 2017. Halyomorpha halys mortality and sublethal feeding effects following insecticide exposure. Journal of Pest Science. 90(4):1257–1268. https://doi.org/10.1007/s10340-017-0871-y.

Cordeiro EMG, de Moura ILT, Fadini MAM, Guedes RNC. 2013. Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere. 93(6):1111–1116.


da Silva WR, Pereira RC, Mendonça LVP, Peçanha LS, de Sales Abreu LM, Abib PHN, Samuels RI, Picanço MC, Silva GA. 2022. Lethal and sublethal effects of insecticides used in the management of Plutella xylostella (Lepidoptera: Plutellidae) on the predator Cycloneda sanguinea L. (Coleoptera: Coccinellidae). Pest Management Science. 78(10):4397-4406. https://doi.org/https://doi.org/10.1002/ps.7060.

de Castro AA, Legaspi JC, Tavares WDS, Meagher RL, Miller N, Kanga L, Haseeb M, Serrão JE, Wilcken CF, Zanuncio JC. 2018. Lethal and behavioral effects of synthetic and organic insecticides on Spodoptera exigua and its predator Podisus maculiventris. PLoS One. 13(11):e0206789. https://doi.org/10.1371/journal.pone.0206789.

Desneux N, Decourtye A, Delpuech J-M. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology. 52(1):81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440.

Finney DJ. 1971. Probit Analysis (3rd Edition ed.). Cambridge University Press. https://onlinelibrary.wiley.com/doi/abs/10.1002/jps.3030411125

Greene JK, Baum JA, Benson EP, Bundy CS, Jones WA, Kennedy GG, McPherson JE, Musser FR, Reay-Jones FPF, Toews MD, et al. 2018. General insect management. In: McPherson JE, editor. Invasive Stink Bugs and Related Species (Pentatomoidea). CRC Press. pp 729–774. https://doi.org/10.1201/9781315371221-16.

Guedes RNC, Cutler GC. 2014. Insecticide-induced hormesis and arthropod pest management. Pest Management Science. 70(5):690–697. https://doi.org/10.1002/ps.3669.

Haddi K, Mendes MV, Barcellos MS, Lino-Neto J, Freitas HL, Guedes RNC, Oliveira EE. 2016. Sexual success after stress? Imidacloprid-induced hormesis in males of the Neotropical stink bug Euschistus heros. PLoS One. 11(6):e0156616. https://doi.org/10.1371/journal.pone.0156616.

Haddi K, Mendonça LP, Dos Santos MF, Guedes RNC, Oliveira EE. 2015. Metabolic and behavioral mechanisms of indoxacarb resistance in Sitophilus zeamais (Coleoptera: curculionidae). Journal of Economic Entomology. 108(1):362–369. https://doi.org/10.1093/jee/tou049.

Haynes KF. 1988. Sublethal effects of neurotoxic insecticides on insect behavior. Annual Review of Entomology. 33(1):149–168. https://doi.org/10.1146/annurev.en.33.010188.001053.

Hlina BL. 2020. ecotox: Analysis of ecotoxicology. R package version 1.4.2.

Huber DPW, Erickson ML, Leutenegger CM, Bohlmann J, Seybold SJ. 2007. Isolation and extreme sex-specific expression of cytochrome P450 genes in the bark beetle, Ips paraconfusus, following feeding on the phloem of host ponderosa pine, Pinus ponderosa. Insect Molecular Biology. 16(3):335–349. https://doi.org/10.1111/j.1365-2583.2007.00731.x.

Hulbert D, Isaacs R, Vandervoort C, Wise JC. 2011. Rainfastness and residual activity of insecticides to control Japanese beetle (Coleoptera: Scarabaeidae) in grapes. Journal of Economic Entomology. 104(5):1656–1664. https://doi.org/10.1603/EC11077.

Kassambara A, Kosinski M. 2018. “Survminer”: Drawing Survival Curves using “ggplot2”. R package version 0.4.2. https://CRAN.R-project.org/package=survminer

Koo H-N, Lee S-W, Yun S-H, Kim HK, Kim G-H. 2015. Feeding response of the cotton aphid, Aphis gossypii, to sublethal rates of flonicamid and imidacloprid. Entomologia Experimentalis et Applicata. 154(2):110–119. https://doi.org/10.1111/eea.12260.

Lee D-H, Nielsen AL, Leskey TC. 2014. Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) evaluated under laboratory and field conditions. Journal of Insect Behaviour. 27(5):639–651. https://doi.org/10.1007/s10905-014-9456-2.

Lee D-H, Short BD, Nielsen AL, Leskey TC. 2014. Impact of organic insecticides on the survivorship and mobility of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in the laboratory. Florida Entomologist. 97(2):414–421. https://doi.org/10.1653/024.097.0211.

Leskey TC, Lee D-H, Short BD, Wright SE. 2012. Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): Analysis of insecticide lethality. Journal of Economic Entomology. 105(5):1726–1735. https://doi.org/10.1603/EC12096.

Li W, Lu Z, Li L, Yu Y, Dong S, Men X, Ye B. 2018. Sublethal effects of imidacloprid on the performance of the bird cherry-oat aphid Rhopalosiphum padi. PLoS One. 13(9):e0204097. https://doi.org/10.1371/journal.pone.0204097.

Lu Z, Dong S, Li C, Li L, Yu Y, Men X, Yin S. 2020. Sublethal and transgenerational effects of dinotefuran on biological parameters and behavioural traits of the mirid bug Apolygus lucorum. Scientific Reports. 10(1):226–234. https://doi.org/10.1038/s41598-019-57098-z.

Maia JB, Carvalho GA, Medina P, Garzón A, Gontijo PDC, Viñuela E. 2016. Lethal and sublethal effects of pesticides on Chrysoperla carnea larvae (Neuroptera: Chrysopidae) and the influence of rainfastness in their degradation pattern over time. Ecotoxicology. 25(5):845–855. https://doi.org/10.1007/s10646-016-1641-y.

McPherson JE (ed). 2018. Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry, and Management. Oxford University Press. https://doi.org/10.1201/

McPherson JE, McPherson RM. 2000. Stink bugs of economic importance in America North of Mexico. CRC Press. https://doi.org/10.1201/9781420042429.

Mittapelly P, Bansal R, Michel A. 2019. Differential expression of cytochrome P450 CYP6 genes in the brown marmorated stink bug, Halyomorpha halys (Hemiptera: pentatomidae). Journal of Economic Entomology. 112(3):1403–1410. https://doi.org/10.1093/jee/toz007.

Morales JA, Cardoso DG, Della Lucia TMC, Guedes RNC. 2013. Weevil x insecticide: Does ‘personality’ matter? PLoS One. 8(6):e67283. https://doi.org/10.1371/journal.pone.0067283.

Morrison WR 3rd, Poling B, Leskey TC. 2017. The consequences of sublethal exposure to insecticide on the survivorship and mobility of Halyomorpha halys (Hemiptera: pentatomidae). Pest Management Science. 73(2):389–396. https://doi.org/10.1002/ps.4322.

Müller C. 2018. Impacts of sublethal insecticide exposure on insects — facts and knowledge gaps. Basic and Applied Ecology. 30:1–10. https://doi.org/10.1016/j.baae.2018.05.001.

Musasia FK, Isaac AO, Masiga DK, Omedo IA, Mwakubambanya R, Ochieng R, Mireji PO. 2013. Sex-specific induction of CYP6 cytochrome P450 genes in cadmium and lead tolerant Anopheles gambiae. Malaria Journal. 12(1):97. https://doi.org/10.1186/1475-


Nielsen AL, Shearer PW, Hamilton GC. 2008. Toxicity of insecticides to Halyomorpha halys (Hemiptera: Pentatomidae) using glass-vial bioassays. Journal of Economic Entomology. 101(4):1439–1442. https://doi.org/10.1603/0022-0493(2008)101.

Ogle DH, Doll JC, Wheeler AP, Dinno A. 2023. FSA: Simple Fisheries Stock Assessment Methods. R package version 0.9.4. https://fishr-core-team.github.io/FSA/.

Pazini JB, Padilha AC, Cagliari D, Bueno FA, Rakes M, Zotti MJ, Martins JFS, Grützmacher AD. 2019. Differential impacts of pesticides on Euschistus heros (Hem.: Pentatomidae) and its parasitoid Telenomus podisi (Hym.: Platygastridae). Scientific Reports. 9(1):6544.


Qu Y, Ullah F, Luo C, Monticelli LS, Lavoir A-V, Gao X, Song D, Desneux N. 2020. Sublethal effects of beta-cypermethrin modulate interspecific interactions between specialist and generalist aphid species on soybean. Ecotoxicology and Environmental Safety. 206:111302. https://doi.org/10.1016/j.ecoenv.2020.111302.

Qu Y, Xiao D, Li J, Chen Z, Biondi A, Desneux N, Gao X, Song D. 2015. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology. 24(3):479–487. https://doi.org/10.1007/s10646-014-1396-2.

Robertson JL, Savin NE, Savin NE, Preisler HK. 2007. Bioassays with Arthropods, 2nd edition. Boca Raton: CRC Press. https://doi.org/10.1201/9781420004045.

SAMAC. 2022. Registered products and MRLs. [accessed 2022, Jan 10]. https://samac.org.za/registered-products. Registration required.

Santos MF, Santos RL, Tomé HVV, Barbosa WF, Martins GF, Guedes RNC, Oliveira EE. 2016. Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros. Journal of Pest Science. 89(1):231–240. https://doi.org/10.1007/s10340-015-0666-y.

Schoeman PS. 2013. Phytophagous stink bugs (Hemiptera: Pentatomidae; Coreidae) associated with macadamia in South Africa. Open Journal of Animal Sciences. 3(3):179–183.


Schoeman PS. 2014b. Aspects affecting distribution and dispersal of the indigenous Heteroptera complex (Heteroptera: Pentatomidae & Coreidae) in South African macadamia orchards. African Entomology. 22(1):191–196. https://doi.org/10.4001/003.022.0130.

Schoeman PS. 2014a. Stink bug IPM on macadamias in South Africa: current status and the road ahead. Trends in Entomology. 10:87–95.

Schoeman PS. 2018. Relative seasonal occurrence of economically significant Heteropterans (Pentatomidae and Coreidae) on macadamias in South Africa: implications for management. African Entomol. 26(2):543–549. https://doi.org/10.4001/003.026.0543.

Schoeman PS. 2020. Damage potential of indigenous Heteroptera species occurring on Macadamia nuts (Macadamia integrifolia Maiden & Betche & Macadamia tetraphylla L. Johnson) in South Africa during the early and late season. International Journal of Tropical Insect Science. 40(1):217–219. https://doi.org/10.1007/s42690-019-00041-6.

Snodgrass GL, Adamczyk JJ Jr, Gore J. 2005. Toxicity of insecticides in a glass-vial bioassay to adult brown, green, and Southern green stink bugs (Heteroptera: pentatomidae). Journal of Economic Entomology. 98(1):177–181. https://doi.org/10.1093/jee/98.1.177.

Somavilla JC, Reis AC, Gubiani PDS, Godoy DN, Stürmer GR, Bernardi O. 2020. Susceptibility of Euschistus heros and Dichelops furcatus (Hemiptera: Pentatomidae) to selected insecticides in Brazil. Journal of Economic Entomology. 113(2):924–931. https://doi.org/10.1093/jee/toz340.

Sonnekus B, Slippers B, Hurley BP, Joubert E, Stiller M, Fourie G. 2022. Diversity and molecular barcoding of stink bugs (Hemiptera: Pentatomidae) associated with macadamia in South Africa. Insects. 13(7):601. https://doi.org/10.3390/insects13070601.

Sosa-Gómez DR, Da Silva JJ, De Oliveira Negrao Lopes I, Corso IC, Almeida AMR, Piubelli De Moraes GC, Baur ME. 2009. Insecticide susceptibility of Euschistus heros (Heteroptera: Pentatomidae) in Brazil. Journal of Economic Entomology. 102(3):1209–1216.


Sosa‐Gómez DR, Corrêa‐Ferreira BS, Kraemer B, Pasini A, Husch PE, Delfino Vieira CE, Reis Martinez CB, Negrão Lopes IO. 2020. Prevalence, damage, management and insecticide resistance of stink bug populations (Hemiptera: Pentatomidae) in commodity crops. Agricultural and Forest Entomology. 22(2):99–118.


Sparks ME, Bansal R, Benoit JB, Blackburn MB, Chao H, Chen M, Cheng S, Childers C, Dinh H, Doddapaneni HV, et al. 2020. Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest. BMC Genomics. 21(1):227.


Stark JD, Banks JE. 2003. Population-level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology. 48(1):505–519. https://doi.org/10.1146/annurev.ento.48.091801.112621.

Tan Y, Biondi A, Desneux N, Gao X-W. 2012. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology. 21(7):1989–1997. https://doi.org/10.1007/s10646-012-0933-0.

Therneau T. 2015. “Survival”: A Package for Survival Analysis in S. R package version 2.38. https://CRAN.R-project.org/package=survival

Tillman PG, Mullinix BG. 2004. Comparison of susceptibility of pest Euschistus servus and predator Podisus maculiventris (Heteroptera: Pentatomidae) to selected insecticides. Journal of Economic Entomology. 97(3):800–806. https://doi.org/10.1603/0022-0493


Tuelher ES, da Silva ÉH, Rodrigues HS, Hirose E, Guedes RNC, Oliveira EE. 2018. Area-wide spatial survey of the likelihood of insecticide control failure in the neotropical brown stink bug Euschistus heros. Journal of Pest Science. 91(2):849–859. https://doi.org/10.1007/s10340-017-0949-6.

Vilca Mallqui KS, Vieira JL, Guedes RNC, Gontijo LM. 2014. Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: bruchinae). Journal of Economic Entomology. 107(2):860–866. https://doi.org/10.1603/EC13526.

Wang L-P, Shen J, Ge L-Q, Wu J-C, Yang G-Q, Jahn GC. 2010. Insecticide-induced increase in the protein content of male accessory glands and its effect on the fecundity of females in the brown planthopper Nilaparvata lugens Stål (Hemiptera: delphacidae). Crop Protection. 29(11):1280–1285. https://doi.org/10.1016/j.cropro.2010.07.009.

Wheeler MW, Park RM, Bailer AJ. 2006. Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environmental Toxicology and Chemistry. 25(5):1441–1444.


Wu H-M, Feng H-L, Wang G-D, Zhang L-L, Zulu L, Liu Y-H, Zheng Y-L, Rao Q. 2022. Sublethal effects of three insecticides on development and reproduction of Spodoptera frugiperda (Lepidoptera: noctuidae). Agronomy (Basel). 12(6):1334. https://doi.org/10.3390/agronomy12061334.

Xu L, Zhao C-Q, Zhang Y-N, Liu Y, Gu Z-Y. 2016. Lethal and sublethal effects of sulfoxaflor on the small brown planthopper Laodelphax striatellus. Journal of Asia-Pacific Entomology. 19(3):683–689. https://doi.org/10.1016/j.aspen.2016.06.013.

Yuan H-B, Li J-H, Liu Y-Q, Cui L, Lu Y-H, Xu X-Y, Li Z, Wu K-M, Desneux N. 2017. Lethal, sublethal and transgenerational effects of the novel chiral neonicotinoid pesticide cycloxaprid on demographic and behavioral traits of Aphis gossypii (Hemiptera: aphididae). Insect Science. 24(5):743–752. https://doi.org/10.1111/1744-7917.12357.

Zeng X, He Y, Wu J, Tang Y, Gu J, Ding W, Zhang Y. 2016. Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: aphididae). Journal of Economic Entomology. 109(4):1595–1602.


Zhou C, Liu L, Yang H, Wang Z, Long G-y, Jin D. 2017. Sublethal effects of imidacloprid on the development, reproduction, and susceptibility of the white-backed planthopper, Sogatella furcifera (Hemiptera: delphacidae). Journal of Asia-Pacific Entomology. 20(3):996–1000. https://doi.org/10.1016/j.aspen.2017.07.002.

Zuo Y-H, Chen M-E. 2014. Differential gene expression in male and female fat body in the oriental fruit fly, Bactrocera dorsalis. Archives of Insect Biochemistry and Physiology. 85(1):48–59. https://doi.org/10.1002/arch.21142.




How to Cite

Elisa E, Allison JA, Hurley B, Slippers B, Fourie G. Lethal and sublethal effects of insecticides on Bathycoelia distincta (Heteroptera: Pentatomidae). Afr. Entomol. [Internet]. 2024 Apr. 5 [cited 2024 May 27];32. Available from: https://www.africanentomology.com/article/view/16992