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Lethal and sublethal effects of three insecticides on the aphid parasitoid, Lysiphlebus fabarum Marshall (Hymenoptera: Aphidiidae)

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Abstract

Lysiphlebus fabarum Marshall is the main parasitoid of the black bean aphid, Aphis fabae Scopoli. Lethal and sublethal effects of insecticides, thiacloprid+deltamethrin, pirimicarb and pymetrozine were evaluated on the parasitoid under laboratory conditions. One-day-old mummies were exposed to the recommended field concentration of either insecticides via dipping method. Adult emergences were reduced by 82.67, 19.98 and 10.67 % for thiacloprid+deltamethrin, pirimicarb and pymetrozine treatments, respectively. Thiacloprid+deltamethrin had the most adverse effect on the fecundity of the emerged females, while pirimicarb and pymetrozine did not have such effects. According to International organization for biological control (IOBC) insecticide toxicity classification, thiacloprid+deltamethrin resulted to be moderately harmful (E = 97.39%), whereas pirimicarb (E = 15.78%) and pymetrozine (E = 5.15%) were harmless. Thiacloprid+deltamethrin negatively affected five of the estimated demographic parameters (GRR, R 0 , r m , λ and T ). Pirimicarb negatively affected GRR, R 0 and T, while it had no adverse effects on r m and λ. None of the studied demographic parameters were affected by pymetrozine. Our results suggest that pirimicarb and pymetrozine can be considered as safe for L. fabarum, but that thiacloprid+deltamethrin can have serious detrimental of this parasitoid in the field.

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References

  • Abbott, W. S. (1925). A method for computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265–267.

    Article  CAS  Google Scholar 

  • Abdulhay, H. S., & Rathi, M. H. (2014). Effect of some insecticides on the egg parasitoid, Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Journal of Al-Nahrain University, 17, 116–123.

    Google Scholar 

  • Acheampong, S., & Stark, J. D. (2004). Effects of the agricultural adjuvant Sylgard 309 and the insecticide pymetrozine on demographic parameters of the aphid parasitoid, Diaeretiella rapae. Biological Control, 31, 133–137.

    Article  CAS  Google Scholar 

  • Almasi, A. (2011). Sublethal effects of insecticides Proteus and Pymetrozine on life table parameters of on lady beetle Hippodamia vaiegata (Goeze) (Col.: Coccinellidae). M. Sc. dissertation. College of Agriculture, University of Tehran, Iran (In Farsi).

  • Almasi, A., Sabahi, Q., Talebi, K. h., & Mardani, A. (2013). Laboratory evalution of the toxicity of Proteus, pymetrozine, deltamethrin and pirimicarb on lady beetle Hippodamia vaiegata (Goeze) (Col.: Coccinellidae). Journal of Plant Protection Research, 53, 143–147.

    Article  CAS  Google Scholar 

  • Baghery-Matin, S. h. (2005). Biology of parasitoid Lysiphlebus fabarum (Hym: Aphidiidae) under laboratory conditions . M. Sc. dissertation. College of Agriculture, Guilan University, Iran (In Farsi).

  • Bayer Crop Science. (2012). Proteus. http://www.bayercropscience.co.nz/. Accessed 4 June 2013.

  • Bayram, A., Onofri, A., Salerno, G., & Conti, E. (2010). Lethal and sublethal effects of preimaginal treatments with two pyrethroids on the life history of the egg parasitoid Telenomus busseolae. BioControl, 55, 697–710.

    Article  CAS  Google Scholar 

  • Biondi, A., Campolo, O., Desneux, N., Siscaro, G., Palmeri, V., & Zappala, L. (2015). Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere, 128, 142–147.

    Article  CAS  PubMed  Google Scholar 

  • Biondi, A., Desneux, N., Amiens-Desneux, E., Siscaro, G., & Zappala, L. (2013a). Biology and developmental strategies of the palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Economic Entomology, 106, 1638–1647.

    Article  PubMed  Google Scholar 

  • Biondi, A., Desneux, N., Siscaro, G., & Zappala, L. (2012a). Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphera, 2012, 803–812.

    Article  Google Scholar 

  • Biondi, A., Mommaerts, V., Smagghe, G., Vinuela, E., Zappala, L., & Desneux, N. (2012b). The non-target impact of spinosyns on beneficial arthropods. Pest Management Science, 68, 1523–1536.

    Article  CAS  PubMed  Google Scholar 

  • Biondi, A., Zappala, L., Stark, J. D., & Desneux, N. (2013b). Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE, 8(9), e76548. doi:10.1371/journal.pone.0076548.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blackman, R. L., & Eastop, V. F. (2000). Aphids on the world's crops, An identification and information guide. London, DC: The Natural History Museum.

    Google Scholar 

  • Borgemeister, C., Poehling, H. M., Dinter, A., & Höller, C. (1993). Effects of insecticides on life history parameters of the aphid parasitoid Aphidius rhopalosiphi [Hym.: Aphidiidae]. Entomophaga, 38, 245–255.

    Article  CAS  Google Scholar 

  • Candolfi, M. P., Barrett, K. L., Campbell, P., Forester, R., Grandy, N., Huet, M. C., Lewis, G., Oomen, P. A., Schmuck, R., & Vogt, H. (2001). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. In SETAC/ESCORT(European Standard Characteristics of non-target arthropod Regulatory Testing) 2nd Workshop report, 21-23 march 2000, Wageningen.

  • Chi, H. (2005). TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/Ecology/Download/Twosex-MSChart.zip/. Accessed 5 July 2013.

  • Chi, H., & Liu, H. (1985). Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 24, 225–240.

    Google Scholar 

  • Desneux, N., Rafalimanana, H., & Kaiser, L. (2004). Doseresponse relationship in lethal and behavioural effects of different insecticides on the parasitic wasp Aphidius ervi. Chemosphere, 54, 619–627.

    Article  CAS  PubMed  Google Scholar 

  • Desneux, N., Ramirez-Romero, R., & Kaiser, L. (2006). Multi-step bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environmental Toxicology and Chemistry, 25, 2675–2682.

    Article  CAS  PubMed  Google Scholar 

  • Forbes, V. E., & Calow, P. (1999). Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environmental Toxicology and Chemistry, 18, 1544–1556.

    Article  CAS  Google Scholar 

  • Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicoloredasian Asian lady beetle (Coleoptera: Coccinellidae). Biological Control, 34,108–114.

  • Hassan, S. A. (1994). Activities of the IOBC/WPRS working group pesticides and beneficial organisms. IOBC/WPRS Bull, 17, 1–5.

    Google Scholar 

  • Hassan, S. A. (1998). The initiative of the IOBC/WPRS working group on pesticides and beneficial organisms. In P. T. Haskell & P. McEwen (Eds.), Ecotoxicology: pesticides and beneficial organisms (pp. 22–27). the Netherlands: Kluwer Academic Publisher.

    Chapter  Google Scholar 

  • Hewa-Kapuge, S., McDougall, S., & Hoffmann, A. (2003). Effects of methoxyfenozide, indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma nr. brassicae (Hymenoptera: Trichogrammatidae) under laboratory and field conditions. Journal of Economic Entomology, 96, 1083–1090.

    Article  CAS  PubMed  Google Scholar 

  • Jansen, J. P. (1996). Side effects of insecticides on Aphidius rhopalosiphi (Hym.: Aphidiidae) in the laboratory. Entomophaga, 41, 37–43.

    Article  CAS  Google Scholar 

  • Jansen, J. P., Defrance, T., & Warnier, A. M. (2011). Sideeffects offlonicamide and pymetrozine on five aphid natural enemys pecies. BioControl, 56, 759–770.

    Article  CAS  Google Scholar 

  • Kanzaki, S. h., & Tanaka, T. (2010). Different responses of a solitary (Meteorus pulchricornis) and a gregarious (Cotesia kariyai) endoparasitoid to four insecticides in the host Pseudaletia separata. Journal of Pest Science, 35, 1–9.

    Article  CAS  Google Scholar 

  • Kheradmand, K., Khosravian, M., & Shahrokhi, S. (2012). Side effect of four insecticides on demographic statistics of aphid parasitoid, Diaeretiella rapae (McIntosh) (Hym., Braconidae). Annals of Biological Research, 3, 3340–3345.

    CAS  Google Scholar 

  • Liu, T. X., Zhang, Y., Peng, L., Rojas, P., & Trumble, J. T. (2012). Risk Assessment of Selected Insecticides on Tamarixia triozae (Hymenoptera: Eulophidae), a Parasitoid of Bactericera cockerelli (Hemiptera: Trizoidae). Journal of Economic Entomology, 105, 490–496.

    Article  CAS  PubMed  Google Scholar 

  • Medina, P., Morales, J. J., Budia, F., Adan, A., Del Estal, P., & Vinuela, E. (2007). Compatibility of endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) protected stages with five selected insecticides. Journal of Economic Entomology, 100, 1789–1796.

    Article  CAS  PubMed  Google Scholar 

  • Moens, J., Tirry, L., & Clercq, P. (2012). Susceptibility of cocooned pupae and adults of the parasitoid Microplitis mediator to selected insecticides. Phytoparasitica, 40, 5–9.

    Article  Google Scholar 

  • Morita, M., Ueda, T., Yoneda, T., Koyanagi, T., & Haga, T. (2007). Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding. Pest Management Science, 63, 969–973.

    Article  CAS  PubMed  Google Scholar 

  • Nuessly, G. S., Hentz, M. G., Beiriger, R., & Scully, B. T. (2004). Insects associated with faba bean, Vicia faba (Fabales: Fabaceae), in southern Florida. Florida Entomologist, 87, 204–211.

    Article  Google Scholar 

  • Preetha, G., Stanley, J., Suresh, S., Kuttalam, S., & Samiyappan, R. (2009). Toxicity of selected insecticides to Trichogramma chilonis: assessing their safety in the rice ecosystem. Phytoparasitica, 37, 209–215.

    Article  CAS  Google Scholar 

  • Purhematy, A., Ahmadi, K., & Moshrefi, M. (2013). Toxicity of Thiacloprid and Fenvalerate on the black bean aphid, Aphis fabae, and biosafety against its parasitoid, Lysiphlebus fabarum. Juornal of Biopesticides, 6, 207–210.

    CAS  Google Scholar 

  • Rasekh, A., Michaud, J. P., Allahyari, H., & Sabahi, Q. (2010). The foraging behavior of Lysiphlebus fabarum (Marshall), a thelytokous parasitoid of the black bean aphid in Iran. Journal of Insect Behavior, 23, 165–179.

    Article  Google Scholar 

  • Raymond, B. A., Darby, C., & Douglas, A. E. (2000). Intraguild predators and the spatial distribution of a parasitoid. Oecologia, 124, 367–372.

    Article  Google Scholar 

  • Sabahi, Q., Rasekh, A., & Michaud, J. P. (2011). Toxicity of three insecticides to Lysiphlebus fabarum, a parasitoid of the black bean aphid Ahis fabae. Journal of Insect Science, 11, 104–112.

    Article  PubMed Central  PubMed  Google Scholar 

  • Saber, M. (2011). Acute and population level toxicity of imidacloprid and fenpyroximate on an important egg parasitoid, Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). Ecotoxicology, 20, 1476–1484.

    Article  CAS  PubMed  Google Scholar 

  • Saber, M., & Abedi, Z. (2013). Effects of methoxyfenozide and pyridalyl on the larval ectoparasitoid Habrobracon hebetor. Journal of Pest Science, 86, 685–693.

    Article  Google Scholar 

  • Sarfraz, M., & Keddie, B. A. (2005). Conserving the efficacy of insecticides against Plutella xylostella (L.) (Lep., Plutellidae). Journal of Applied Entomology, 129, 149–157.

    Article  CAS  Google Scholar 

  • SPSS. (2004). SPSS 14.0 for windows. Chicago, IL, USA.

  • Stara, J., Ourednicjova, J., & Kocourek, F. (2011). Laboratory evaluation of the side effects of insecticides on Aphidius colemani (Hymenoptera: Aphidiidae), Aphidoletes aphidimyza (Diptera: Cecidomyiidae), and Neoseiulus cucumeris (Acari: Phytoseidae). Journal of Pest Science, 84, 25–31.

    Article  Google Scholar 

  • Stark, J. D., & Banks, J. E. (2003). Population level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48, 505–519.

    Article  CAS  PubMed  Google Scholar 

  • Stark, J. D., Banks, J. E., & Acheampong, S. (2004). Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure. Biological Control, 29, 392–398.

    Article  Google Scholar 

  • Symington, C. A. (2003). Lethal and sublethal effects of pesticides on the potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera:Gelechiidae) and its parasitoid Orgilus lepidus Muesebeck (Hymenoptera:Braconidae). Crop Protection, 22, 513–519.

    Article  CAS  Google Scholar 

  • Tran, D. H., Takagi, M., & Takasu, K. (2004). Effects of selective insecticides on host searching and oviposition behavior of Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae), a larval parasitoid of the American serpentine leafminer. Applied Entomology and Zoology, 39, 435–444.

    Article  CAS  Google Scholar 

  • Umoru, P. A., & Powell, W. (2002). Sublethal effects of the insecticides pirimicarb and dimethoate on the aphid parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) when attacking and developing in insecticide-resistant hosts. Biocontrol Science and Technology, 12, 605–614.

    Article  Google Scholar 

  • Vogt, H., Bigler, F., Brown, K., Candolfi, M. P., Kemmeter, F., Kuhner, C. h., Moll, M., Travis, A., Ufer, A., Vinuela, E., Waldburger, M., & Waltersdorfer, A. (2000). Laboratory method to test effects of plant protection products on larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). In M. P. Candolfi, S. Blumel, R. Forster, F. M. Bakker, C. Grimm, S. A. Hassan, U. Heimbach, M. A. Mead-Briggs, B. Reber, R. Schmuck, & H. Vogt (Eds.), Guide lines to evaluate side-effects of plant protection products to non-target arthropods (pp. 27–44). Gent: IOBC/WPRS.

    Google Scholar 

  • Völkl, W., & Stechman, D. H. (1998). Parasitism of the black bean aphid (Aphis fabae) by Lysiphlebus fabarum (Hymenoptera: Aphidiidae): the influence of host plant and habitat. Journal of Applied Entomology, 122, 201–206.

    Article  Google Scholar 

  • Wright, D. J., & Verkert, R. H. J. (1995). Integration of chemical and biological control systems for arthropods; evaluation in a multitrophic context. Pesticides Science, 44, 207–218.

    Article  CAS  Google Scholar 

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Acknowledgement

We would like to acknowledge the financial support of University of Tehran for this research under grant number 73131676-6-03. This research project was funded in part by the Center of Excellence in Plant Protection, Ministry of Science, Research, and Technology, Iran.

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Correspondence to Ardavan Mardani.

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Mardani, A., Sabahi, Q., Rasekh, A. et al. Lethal and sublethal effects of three insecticides on the aphid parasitoid, Lysiphlebus fabarum Marshall (Hymenoptera: Aphidiidae). Phytoparasitica 44, 91–98 (2016). https://doi.org/10.1007/s12600-015-0502-1

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