Abstract
Botanical insecticides (BIs) are considered a valuable alternative for plant protection in sustainable agriculture. The use of both BIs and parasitoids are presumed to be mutually compatible pest management practices. However, there is controversy on this subject, as various studies have reported lethal and sublethal effects of BIs on hymenopteran parasitoids. To shed new light on this controversy, a meta-analytic approach of the effects of BIs on adult mortality, parasitism, and parasitoid emergence under laboratory conditions was performed. We show that BIs increased mortality, decreased parasitism, and decreased parasitoid emergence. Botanical insecticides derived from Nicotiana tabacum and Caceolaria andina were particulary lethal. Most of the parasitoid groups showed susceptibility to BIs, but the families Scelionidae and Ichneumonidae were not significantly affected. The negative effects of BIs were seen regardless of the type of exposure (topical, ingestion, or residual). In conclusion, this meta-analysis showed that under laboratory conditions, exposure of hymenopteran parasitoids to BIs had significant negative effects on adult mortality, parasitism, and parasitoid emergence.
Similar content being viewed by others
References
Abdel-Sattar E, Zaitoun AA, Farag MA, Gayed SHE, Harraz FM (2010) Chemical composition, insecticidal and insect repellent activity of Schinus molle L. leaf and fruit essential oils against Trogoderma granarium and Tribolium castaneum. Nat Prod Res 24(3):226–235. https://doi.org/10.1080/14786410802346223
Akhtar Y, Isman MB, Lee CH, Lee SG, Lee HS (2012) Toxicity of quinones against two-spotted spider mite and three species of aphids in laboratory and greenhouse conditions. Ind Crop Prod 37(1):536–541. https://doi.org/10.1016/j.indcrop.2011.07.033
Almeida GD, Zanuncio JC, Pratissoli D, Andrade GS, Cecon PR, Serrão JE (2010) Effect of azadirachtin on the control of Anticarsia gemmatalis and its impact on Trichogramma pretiosum. Phytoparasitica 38(5):413–419. https://doi.org/10.1007/s12600-010-0124-6
Babu TH, Rao VRS, Tiwari AK, Babu KS, Srinivas PV, Ali AZ, Rao JM (2008) Synthesis and biological evaluation of novel 8-aminomethylated oroxylin A analogues as α-glucosidase inhibitors. Bioorg Med Chem Lett 18(5):1659–1662. https://doi.org/10.1016/j.bmcl.2008.01.055
Baughman DS, Moore DW, Scott GI (1989) A comparison and evaluation of field and laboratory toxicity tests with fenvalerate on an estuarine crustacean. Environ Toxicol Chem 8(5):417–429. https://doi.org/10.1002/etc.5620080508
Blümel S, Makker F, Grove A (1993) Evaluation of different methods to assess the side-effects of pesticides on Phytoseiulus persimilis A.-H. Exp Appl Acarol 17(3):161–169. https://doi.org/10.1007/BF00118433
Boeke SJ, Sinzogan AA, De Almeida RP, De Boer PW, Jeong G, Kossou DK, Van Loon JJ (2003) Side-effects of cowpea treatment with botanical insecticides on two parasitoids of Callosobruchus maculatus. Entomol Exp Appl 108(1):43–51. https://doi.org/10.1046/j.1570-7458.2003.00066.x
Bostanian NJ, Akalach M, Chiasson H (2005) Effects of a Chenopodium-based botanical insecticide/acaricide on Orius insidiosus (Hemiptera: Anthocoridae) and Aphidius colemani (Hymenoptera: Braconidae). Pest Manag Sci 61(10):979–984. https://doi.org/10.1002/ps.1065
Chiasson H, Vincent C, Bostanian NJ (2004) Insecticidal properties of a Chenopodium-based botanical. J Econ Entomol 97(4):1378–1383. https://doi.org/10.1093/jee/97.4.1378
Cluasen CP (1978) Introduced parasites and predators of arthropod pest and weeds: a world review. Agriculture Handbook. No. 480, United States Dept. of Agriculture, Washington D. C
Defagó MT, Dumón A, Avalos DS, Palacios SM, Valladares G (2011) Effects of Melia azedarach extract on Cotesia ayerza, parasitoid of the alfalfa defoliator Colias lesbia. Biol Control 57(2):75–78. https://doi.org/10.1016/j.biocontrol.2011.01.002
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52(1):81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Dolphin K, Quicke DJ (2001) Estimating the global species richness of an incompletely described taxon: an example using parasitoid wasps (Hymenoptera: Braconidae). Biol J Linn Soc 73(3):279–228. https://doi.org/10.1111/j.1095-8312.2001.tb01363.x
Dua VK, Pandey AC, Dash AP (2010) Adulticidal activity of essential oil of Lantana camara leaves against mosquitoes. Indian Med Res 131:434–439
El-Wakeil NE (2013) Botanical pesticides and their mode of actions. Gesunde Pflanz 65(4):125–149. https://doi.org/10.1007/s10343-013-0308-3
Gurevitch J, Hedgez LV (2001) Meta-analysis: combining results of independent experiments. Pages 347–369 in Barton, K. E., & Koricheva. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493
Hall DG, Nguyen R (2010) Toxicity of pesticides to Tamarixia radiata, a parasitoid of the Asian citrus psyllid. BioControl 55(5):601–611. https://doi.org/10.1007/s10526-010-9283-0
Haseeb M, Liu TX, Jones WA (2004) Effects of selected insecticides on Cotesia plutellae, endoparasitoid of Plutella xylostella. BioControl 49(1):33–46. https://doi.org/10.1023/B:BICO.0000009377.75941.d7
Hollingworth RM, Ahammadsahib KI, Gadelhak G, McLaughlin JL (1994) New inhibitors of complex I of the mitochondrial electron transport chain with activity as pesticides. Biochem Soc Trans 22(1):230–233. https://doi.org/10.1042/bst0220230
Huerta A, Chiffelle I, Puga K, Azúa F, Araya JE (2010) Toxicity and repellence of aqueous and ethanolic extracts from Schinus molle on elm leaf beetle Xanthogaleruca luteola. Crop Prot 29(10):1118–1123. https://doi.org/10.1016/j.cropro.2010.04.010
Iannacone O, Lamas M (2003) Efectos toxicológicos de extractos de molle (Schinus molle) y lantana (Lantana camara) sobre Chrysoperla externa (Neuroptera: Chrysopidae), Trichogramma pintoi (Hymenoptera: Trichogrammatidae) y Copidosoma koehleri (Hymenoptera: Encyrtidae) en el Perú. Agric Tech 63:347–360
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51(1):45–66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19(3):140–145. https://doi.org/10.1016/j.tplants.2013.11.005
Kostyukovsky M, Rafaeli A, Gileadi C, Demchenko N, Shaaya E (2002) Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci 58(11):1101–1106. https://doi.org/10.1002/ps.548
Kumar P, Whitten M, Thoeming G, Borgemeister C, Poehling HM (2008) Effects of bio-pesticides on Eretmocerus warrae (Hym., Aphelinidae), a parasitoid of Bemisia tabaci (Hom., Aleyrodidae). J Appl Entomol 132(8):605–613. https://doi.org/10.1111/j.1439-0418.2008.01282.x
Kumar P, Singh HP, Poehling H (2010) Effects of neem on adults of Eretmocerus warrae (Hym., Aphelinidae), a parasitoid of Bemisia tabaci (Hom., Aleyrodidae) in tropical horticulture systems. J Plant Dis Protect 117(6):273–277. https://doi.org/10.1007/BF03356373
López M, Pellegriono A, Carrizo P, Dubin M, Stoppani A (2002) Effect of the lipophilic o-naphthoquinone CG 10-248 on rat liver mitochondria structure and function. Biocell 26(2):237–245
Luckmann D, de Gouvea A, Potrich M, da Silva ERL, Puretz B, Dallacort S, Gonçalves TE (2014) Seletividade de produtos naturais comer ciais a Trichogramma pretiosum (Riley, 1879) (Hymenoptera: Trichogrammatidae). Revista Ceres 61(6):924–931. https://doi.org/10.1590/0034-737X201461060006
Montes-Molina JA, Luna-Guido ML, Espinoza-Paz N, Govaerts B, Gutierrez-Miceli FA, Dendooven L (2008) Are extracts of neem (Azadirachta indica A. Juss.(L.)) and Gliricidia sepium (Jacquin) an alternative to control pests on maize (Zea mays L.) ? Crop Prot 27(3-5):763–774. https://doi.org/10.1016/j.cropro.2007.11.002
Perera DR, Armstrong G, Senanayake N (2000) Effect of antifeedants on the diamondback moth (Plutella xylostella) and its parasitoid Cotesia plutellae. Pest Manag Sci 56(5):486–490. https://doi.org/10.1002/(SICI)1526-4998(200005)56:5<486::AID-PS162>3.0.CO;2-O
Regnault-Roger C, Philogène BJ (2008) Past and current prospects for the use of botanicals and plant allelochemicals in integrated pest management. Pharm Biol 46(1-2):41–52. https://doi.org/10.1080/13880200701729794
Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59(2):464–468. https://doi.org/10.1111/j.0014-3820.2005.tb01004.x
Rosenberg MS, Adams DC, Gurevitch J (2002) MetaWin: statistical software for meta-analysis. Version 2.1. Sinauer, Sunderland
Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychcol Bull 86(3):638–641. https://doi.org/10.1037/0033-2909.86.3.638
Simmonds MSJ, Manlove JD, Blaney WM, Khambay BPS (2002) Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporariorum and the parasitoid Encarsia formosa. Entomol Exp Appl 102(1):39–47. https://doi.org/10.1046/j.1570-7458.2002.00923.x
Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34(3):236–246. https://doi.org/10.1016/j.biocontrol.2005.02.017
Studebaker GE, Kring TJ (2003) Effects of insecticides on Orius insidiosus (hemiptera: anthocoridae), measured by field, greenhouse and petri dish bioassays. Fla Entomol 86(2):178–185
Tang YQ, Weathersbee AA, Mayer RT (2002) Effect of neem seed extract on the brown citrus aphid (Homoptera: Aphididae) and its parasitoid Lysiphlebus testaceipes (Hymenoptera: Aphidiidae). Environ Entomol 31(1):172–176. https://doi.org/10.1603/0046-225X-31.1.172
Tunca H, Kilinçer N, Özkan C (2014) Toxicity and repellent effects of some botanical insecticides on the egg-larval parasitoid Chelonus oculator Panzer (Hymenoptera: Braconidae). Sci Res Essays 9:106–113
Xavier VM, Message D, Picanço MC, Chediak M, Santana PA Jr, Ramos RS, Martins JC (2015) Acute toxicity and sublethal effects of botanical insecticides to honey bees. J Insect Sci 15:1–6
Acknowledgments
The authors thank CONACyT Mexico for the M. Sc. scholarship granted to Raul Monsreal Ceballos. Thanks also to the Dr. Maricarmen Sánchez Borja for technical assistance with the experiments for the thesis research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Edison Ryoiti Sujii – Embrapa/Cernagen
Electronic supplementary material
ESM 1
(DOCX 34 kb)
Rights and permissions
About this article
Cite this article
Monsreal-Ceballos, R.J., Ruiz-Sánchez, E., Ballina-Gómez, H.S. et al. Effects of Botanical Insecticides on Hymenopteran Parasitoids: a Meta-analysis Approach. Neotrop Entomol 47, 681–688 (2018). https://doi.org/10.1007/s13744-017-0580-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-017-0580-5