Skip to main content
Log in

Parasitism, host feeding, and transgenerational effects of three insecticides on the eulophid parasitoid Tamarixia triozae when exposed in the immature stages

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The ectoparasitoid Tamarixia triozae is a promising biological control agent of the tomato psyllid, Bactericera cockerelli, based on its high parasitism rates on different crops. The parasitism, host feeding, and transgenerational effects (in terms of sex ratio) of T. triozae females exposed to three insecticides (soybean oil, imidacloprid, and abamectin) as eggs, larvae, and pupae were evaluated when a mixture of second, third, fourth, and fifth instars of the host B. cockerelli was offered. The concentrations bioassayed of each insecticide corresponded to the minimum field-registered concentration [MiFRC] and one-half the MiFRC. No parasitism of B. cockerelli second instars was recorded when parasitoid’s females were exposed in any of the three immature stages to any of the insecticides. In contrast, in some cases, parasitism of T. triozae females treated as eggs, larvae, or pupae with soybean oil and imidacloprid was reduced in third, fourth, or fifth instar. In most cases, the host feeding was reduced in second and third instar of the host B. cockerelli when T. triozae females were treated as eggs, larvae, or pupae. Any insecticide modified the sex ratio in the F2 generation. In conclusion, both parasitism and host feeding were affected by the insecticides depending on the concentration and on the nymphal instar of the host B. cockerelli offered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abreu CM, Moscardini VF, Gontijo PC, Carvalho GA, Lopes de Oliveira R, Nonato de Oliveira H (2014) Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae). Ecotoxicology 23:1399–1408

    Google Scholar 

  • Adán A, Soria S, Del Estal P, Sánchez-Brunete C, Viñuela E (1998) Differential action of two azadirachtin formulations on different developmental stages of Ceratitis capitata. Bol San Veg Plagas 24:1009–1018

    Google Scholar 

  • Amini JN, Saber M (2018) Sublethal effects of imidacloprid and pymetrozine on the functional response of the aphid parasitoid, Lysiphlebus fabarum. Entomol Gen 38:173–190

    Google Scholar 

  • Beloti VH, Alves GR, Dias ADF, Manara PM, Andrade MR, Borges DCG, Yamamoto PT (2015) Lethal and sublethal effects of insecticides used on citrus, on the ectoparasitoid Tamarixia radiata. PLoS One 10:e0132128

    Google Scholar 

  • Benjamin EO, Wesseler JHH (2016) A socioeconomic analysis of biocontrol in integrated pest management: a review of the effects of uncertainty, irreversibility and flexibility. Wageningen J Life Sci 77:53–60

    Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012) Non-target impact of spinosyns on beneficial arthropods, a review. Pest Manag Sci 68:1523–1536

    CAS  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One 8:e76548

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Bravo, M.E., López, L.P., 2007. Principales plagas del chile de agua en los valles centrales de Oaxaca. Agroproduce. http://www.oeidrusoaxaca.gob.mx/produce/abril07/contenido.pdf. Accessed 26 May 2019

  • Burks BD (1943) The north American parasitic wasps of the genus Tetrastichus. A contribution to the biological control of insect pests. U S Natl Mus Proc 93:505–608

    Google Scholar 

  • Camacho-Tapia M, Rojas-Martínez RI, Zavaleta-Mejía E et al (2011) Aetiology of chili pepper variegation from Yurecuaro, Mexico. J Plant Pathol 93:331–335

    Google Scholar 

  • Carvalho FP (2017) Pesticides, environment and food safety. Food Energ Secur 6:48–60

    Google Scholar 

  • Carvalho GA, Godoy MS, Parreira DS, Rezende DT (2010) Effect of chemical insecticides used in tomato crops on immature Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Rev Colomb Entomol 36:10–15

    CAS  Google Scholar 

  • Cerón-González C, Lomelí-Flores JR, Rodríguez-Leyva E, Torres-Ruíz A (2014) Fertility and feeding of Tamarixia triozae (Hymenoptera: Eulophidae) on potato psyllid Bactericera cockerelli. Rev Mex Cienc Agríc 5:893–899

    Google Scholar 

  • Cheng XQ, Cao FQ, Zhang YB, Guo JY, Wan FH, Liu WX (2017) Life history and life table of the host feeding parasitoid Hemiptarsenus varicornis (Hymenoptera: Eulophidae). Appl Entomol Zool 52:287–293

    Google Scholar 

  • Cloyd RA, Bethke JA (2010) Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. Pest Manag Sci 67:3–9

    Google Scholar 

  • Deletre E, Chandre F, Barkman B, Menut C, Martin T (2014) Naturally occurring bioactive compounds from four repellent essential oils against Bemisia tabaci whiteflies. Pest Manag Sci 72:179–189

    Google Scholar 

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

    CAS  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    CAS  Google Scholar 

  • Ehi-Eromosele CO, Nwiniy OC, Ajani OO (2013) Integrated pest management. In: Soloneski S, Larramendy M (eds) Weed and pest control conventional and new challenges. InTechOpen, London, pp 105–115

    Google Scholar 

  • FAO (2017) The Food and Agriculture Organization Corporate Statistical Database. http://www.fao.org/faostat/en/#home. Accessed 20 June 2019

  • Fernández MM, Medina P, Del Estal P, Viñuela E (2010) Testing side-effects of pesticides on the most protected life stage of Eretmocerus mundus (Mercet) (Hymenoptera, Aphelinidae), parasitoid of the whitefly Bemisia tabaci (Gennadius) (Hemiptera, Aleyrodidae) in the laboratory. IOBC/WPRS Bull 55:101–107

    Google Scholar 

  • Fernández MM, Medina P, Fereres A, Smagghe G, Viñuela E (2015) Are mummies and adults of Eretmocerus mundus (Hymenoptera: Aphelinidae) compatible with modern insecticides? J Econ Entomol 108:2268–2277

    Google Scholar 

  • Francesena N, Desneux N, Ribeiro de Campos M, Schneider MI (2017) Side effects of spirotetramat on pupae and adults of a neotropical strain of Eretmocerus mundus (Hymenoptera: Aphelinidae): effects on the life parameters and demography. Environ Sci Pollut Res 24:17719–17730

    CAS  Google Scholar 

  • Garzón-Tiznado JA, Cárdenas-Valenzuela OG, Bujanos-Muñiz R et al (2009) Association of Hemiptera: triozidae with the disease “Permanente del tomate” in Mexico. Agric Téc Méx 35:61–72

    Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticides-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:3.1–3.20

    Google Scholar 

  • Heimpel GE, Collier TR (1996) The evolution of host feeding behaviour in insect parasitoids. Biol Rev 71:373–400

    Google Scholar 

  • Hernández-Moreno S, Pérez-Panduro A, Lomeli-Flores JR et al (2017) Biological fitness of Tamarixia triozae mediated by its host plant. Southwest Entomol 42:225–236

    Google Scholar 

  • Jacas JA, Viñuela E (1994) Side-effects of pesticides on Opius concolor, a parasitoid of the olive fruit fly. IOBC/WPRS Bull 17:143–146

    Google Scholar 

  • Jervis BA, Kidd NAC (1986) Host feeding strategies in hymenopteran parasitoids. Biol Rev 61:395–434

    Google Scholar 

  • Lasota JA, Dybas RA (1991) Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu Rev Entomol 36:91–117

    CAS  Google Scholar 

  • Lee CY (2000) Sublethal effects of insecticides on longevity, fecundity and behaviour of insect pest: a review. J Biosci 11:107–112

    Google Scholar 

  • Lira ACS, Zanardi OZ, Beloti VH, Bordini GP, Yamamoto PT, Parra JR, Carvalho GA (2015) Lethal and sublethal impacts of acaricides on Tamarixia radiata (Hemiptera: Eulophidae), an important ectoparasitoid of Diaphorina citri (Hemiptera: Liviidae). J Econ Entomol 108:2278–2288

    CAS  Google Scholar 

  • Liu TX, Zhang YM, Peng LN, Rojas P, Trumble JT (2012) Risk assessment of selected insecticides on Tamarixia triozae (Hymenoptera: Eulophidae), a parasitoid of Bactericera cockerelli (Hemiptera. Triozidae). J Econ Entomol 105:490–496

    CAS  Google Scholar 

  • Liu WX, Wang WX, Zhang YB, Wang W, Lu SL, Wan FH (2015) Adult diet affects the life history and host-killing behavior of a host feeding parasitoid. Biol Control 81:58–64

    Google Scholar 

  • Lombardi de Carvalho SP (2008) Toxicidade de insecticidas neonicotinoides sobre o psilídeo Diaphorina citri Kuwayama (Hemiptera: Psyllidae) e o parasitódie Tamarixia radiata (Waterson) (Hymenoptera: Eulophidae). Tese Doutorado. Escola Superior de Agricultura “Luiz de Queiroz”. Universidade de Sao Paulo. Sao Paulo, Brasil (In Portuguese)

  • Lomelí-Flores J, Bueno PR (2002) Nuevo registro de Tamarixia triozae (Burks) parasitoide del psílido del tomate Paratrioza cockerelli (Sulc) (Homoptera: Psyllidae) en Mexico. Folia Entomol Mex 41:375–376

    Google Scholar 

  • Lucchi A, Benelli G (2018) Towards pesticide-free farming? Sharing needs and knowledge promotes integrated pest management. Environ Sci Poll Res 25:13439–13445

    Google Scholar 

  • Luna-Cruz A (2014) Toxicity and residuality of insecticides on Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) parasitoid of Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). PhD thesis. College of Postgraduates. Montecillo, Texcoco, Estado de México, Mexico (In Spanish)

  • Luna-Cruz A, Lomelí-Flores R, Rodríguez-Leyva E, Ortega-Arenas LD, Huerta-De la Peña A (2011) Toxicidad de cuatro insecticidas sobre Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) y su hospedero Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). Acta Zool Mex (ns) 27:509–526

    Google Scholar 

  • Luna-Cruz A, Rodríguez-Leyva E, Lomelí-Flores JR, Ortega-Arenas LD, Bautista-Martínez N, Pineda S (2015) Toxicity and residual activity of insecticides against Tamarixia triozae (Hymenoptera: Eulophidae), a parasitoid of Bactericera cockerelli (Hemiptera: Triozidae). J Econ Entomol 108:2289–2295

    CAS  Google Scholar 

  • Martínez AM, Chavarrieta JM, Morales SI et al (2015) Behavior of Tamarixia triozae females (Hymenoptera: Eulophidae) attacking Bactericera cockerelli (Hemiptera: Triozidae) and effects of three pesticides on this parasitoid. Environ Entomol 44:3–11

    Google Scholar 

  • Medina P, Morales J, González-Núñez M, Viñuela E (2008) Is it the use of some selected insecticides compatible with two noctuid endoparasitoids: Hyposoter didymator and Chelonus inanitus? IOBC/WPRS Bull 35:51–59

    Google Scholar 

  • Mohammed AAAH, Desneux N, Fan Y, Han P, Ali A, Song D, Gao XW (2018) Impact of imidacloprid and natural enemies on cereal aphids: integration or ecosystem service disruption? Entomol Gen 37:47–61

    Google Scholar 

  • Morales ASI, Martínez AM, Figueroa JI et al (2013) Parámetros de vida del parasitoide sinovigénico Tamarixia triozae (Hymenoptera: Eulophidae). Rev Colomb Entomol 39:243–249

    Google Scholar 

  • Morales SI, Martínez AM, Viñuela E, Chavarrieta JM, Figueroa JI, Schneider MI, Tamayo F, Pineda S (2018) Lethal and sublethal effects on Tamarixia triozae (Hymenoptera: Eulophidae), an ectoparasitoid of Bactericera cockerelli (Hemiptera: Triozidae), of three insecticides used on solanaceous crops. J Econ Entomol 111:1048–1055

    CAS  Google Scholar 

  • Nafiu BS, Dong H, Cong B (2014) Principles of biological control in integrated pest management. I J A R T 3:104–116

    Google Scholar 

  • Pakyari H, Enkegaard A (2015) Sublethal and transgenerational effects of abamectin on the biological performance of the predatory thrips Scolothrips longicornis (Thysanoptera: Thripidae). J Econ Entomol 108:559–565

    CAS  Google Scholar 

  • Pappas ML, Migkou F, Broufas GD (2013) Incidence of resistance to neonicotinoid insecticides in greenhouse populations of the whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) from Greece. Appl Entomol Zool 48:373–378

    CAS  Google Scholar 

  • Passos LC, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143

    Google Scholar 

  • Pérez-Bernal AL (2018) Efectos letales, subletales y transgeneracionales causados por azadiractina y flufenoxuron sobre el ectoparasitoide Tamarixia triozae (Hymenoptera: Eulophidae). Unpublished Bachelor’s thesis. Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo. Morelia, Michoacán, Mexico

  • Pimentel D (2005) Environmental and economic costs of the application of pesticides primarily in the United States. Environ Dev Sustain 7:229–252

    Google Scholar 

  • Pless CD, Deyton DE, Sams CE (1995) Control of San Jose scale, terrapin scale, and European red mite on dormant fruit trees with soybean oil. Hortic Sci 20:94–97

    Google Scholar 

  • Pulidindi K, Pandey H (2019). Biocontrol agents market size by active substance (microbials [bacteria, fungi, virus, protozoa, yeasts], macro-organism [insects, mites, nematodes], biochemicals [semio-chemicals, plant extracts, plant growth regulators, organic acid]), by crop (fruits & vegetables, cereals and grains, pulses), by application (seed treatment, on-field, post-harvest), regional outlook (U.S., Canada, Germany, UK, France, Spain, Italy, Greece, Sweden, Russia, China, India, Japan, South Korea, Brazil, Mexico, South Africa), growth potential, price trends, competitive market share and forecast, 2019–2025. Global Market Insights ID, GMI1551. https://www.gminsights.com/industry-analysis/biocontrol-agents-market. Accessed 26 September 2019

  • Rafiee-Dastjerdi H, Hassanpour M, Nouri-Ganbalani G, Golizadeh A, Sarmadi S (2012) Sublethal effects of indoxacarb, imidacloprid and deltamethrin on life table parameters of Habrobracon hebetor (Hymenoptera: Braconidae) in pupal stage treatment. J Crop Prot 1:221–228

    Google Scholar 

  • Rojas P, Rodríguez-Leyva E, Lomelí-Flores JR, Tong-Xian L (2015) Biology and life history of Tamarixia triozae, a parasitoid of the potato psyllid Bactericera cockerelli. BioControl 60:27–35

    Google Scholar 

  • Sayed SM, El Amaouty SA, Tabozada EOK (2014) Effects of the neonicotinoid compound, emamectin on Bracon brevicornis (Hymenoptera: Braconidae) with parasitization on two lepidopteran hosts. Life Sci J 11:232–235

    CAS  Google Scholar 

  • Schneider MI, Smagghe G, Gobbi A, Viñuela E (2003) Toxicity and pharmacokinetics of insect growth regulators on pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a parasitoid of early larval instars of Lepidopteran pests. J Econ Entomol 96:1054–1065

    CAS  Google Scholar 

  • Schneider MI, Smagghe G, Pineda S, Viñuela E (2004) Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third-instar larvae of the endoparasitoid Hypososter didymator. Biol Control 31:189–198

    CAS  Google Scholar 

  • Singh S (2015) Impact of new chemistry on biocontrol agents of major crops pests. Int J Agric Sci Vet Med 3:14–33

    Google Scholar 

  • Sohrabi F, Shishehbor P, Saber M, Said MM (2012) Lethal and sublethal effects of buprofezin and imidacloprid on the whitefly parasitoid Encarsia inaron (Hymenoptera: Aphelinidae). Crop Prot 32:83–89

    CAS  Google Scholar 

  • Sohrabi F, Shishehbor P, Saber M, Said MM (2013) Lethal and sublethal effects of buprofezin and imidacloprid on the sweet potato whitefly parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Crop Prot 45:98–103

    CAS  Google Scholar 

  • Stanley J, Preetha G (2016) Pesticide toxicity to parasitoids: exposure, toxicity and risk assessment methodologies. In: Stanly J, Preetha G (eds) Pesticide toxicity to non-target organisms: exposure, toxicity and risk assessment methodologies. Springer Nature, Dordrecht, pp 99–151

    Google Scholar 

  • Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519

    CAS  Google Scholar 

  • Stark JD, Banks JE, Acheampong S (2014) Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure. Biol Control 29:392–398

    Google Scholar 

  • Steiner AA (1984) The universal nutrient solution. In: proceedings 6th international congress on Soilles culture. 29 April to 5 may of 1984. Wageningen. pp 633–650

  • Talebi K, Kavousi A, Sabahi Q (2008) Impacts of pesticides on arthropod biological control agents. Pest Technol 2:87–97

    Google Scholar 

  • Tamayo-Mejía F, Tamez-Guerra P, Guzmán-Franco AW, Gómez-Flores R (2015) Can Beauveria bassiana Bals. (Vuill) (Ascomycetes: Hypocreales) and Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) be used together for improved biological control of Bactericera cockerelli (Hemiptera: Triozidae)? Biol Control 90:42–48

    Google Scholar 

  • Tan Y, Biondi A, Desneux N, Gao XW (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 21:1989–1997

    CAS  Google Scholar 

  • Tang YQ, Huang ZP (1991) Studies on the biology of two primary parasites of Diaphorina citri Kuwayama (Homoptera: Psyllidae). In: proceedings of the, 6th international Asia Pacific workshop on integrated Citrus health management. Kual Lumpur. pp 91–98

  • Taylor SV, Burrack HJ, Roe RM, Bacheler JS, Sorenson CE (2015) Systemic imidacloprid affects intraguild parasitoids differently. PLoS One 10:e0144598

    Google Scholar 

  • Tena A, Planes L, Urbaneja A (2016) Uniformity of petroleum-derived spray oils: lethal and sublethal effects on a herbivore pest and its parasitoid. Agr Forest Entomol 19:294–301

    Google Scholar 

  • Tofangsazi N, Morales-Rodriguez A, Daugherty MP, Simmons GS, Grafton-Cardwell EE (2018) Residual toxicity of selected organic insecticides to Diaphorina citri (Hemiptera: Liviidae) and non-target effects on Tamarixia radiata (Hymenoptera: Eulophidae) in California. Crop Prot 108:62–70

    CAS  Google Scholar 

  • Ueno T (1999) Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch. Evol Ecol 13:33–44

    Google Scholar 

  • van Lenteren J (2012) The state of commercial augmentative biological control: plenty of natural enemies bur a frustrating lack of uptake. BioControl 57:1–20

    Google Scholar 

  • Viñuela E (2005) Biological control: a key element in sustainable agriculture. In: Jacas J, caballero P, Avilla J (eds) biological control of pests, diseases and weeds and the sustainability of agriculture. 15-30 UJI/Universidad Pública Navarra, Pamplona, Spain, pp 15-30 (In Spanish)

  • Werdin GJO, Laumann RA, da Silveira S, Blassioli MMC, Borges M, Ferrero AA (2013) Lethal and sublethal effects of four essential oils on the egg parasitoids Trissolcus basalis. Chemosphere 92:608–615

    Google Scholar 

  • Williams T, Arredondo-Bernal HC, Rodríguez del Bosque LA (2013) Biological pest control in Mexico. Annu Rev Entomol 58:119–140

    CAS  Google Scholar 

  • Yang XB, Zhang YM, Hua L, Peng LN, Munyaneza JE, Trumble JT, Liu TX (2010) Repellency of selected biorational insecticides to potato psyllid, Bactericera cockerelli (Hemiptera: Psyllidae). Crop Prot 29:1320–1324

    Google Scholar 

  • Yang NW, Ji LL, Lövei GL, Wan FH (2012) Shifting preference between oviposition vs host feeding under changing host densities in two aphelinids parasitoids. PLoS One 7:e41189

    CAS  Google Scholar 

  • Yang Y, Beattie AC, Spooner-Hart RN, Huang M, Barchia I, Holford P (2013) Influence of leaf age and type, non-host volatiles, and mineral oil deposits on the incidence, distribution, and form of stylet tracks of Diaphorina citri. Entomol Exp Appl 147:33–49

    CAS  Google Scholar 

  • Zar JH (2014) Biostatistical analysis: Pearson new international edition. Pearson

Download references

Acknowledgments

To the Coordinación de la Investigación Científica, Universidad Michoacana de San Nicolas de Hidalgo. Sinue I. Morales received a student stipend from the Consejo Nacional de Ciencia y Tecnología, Mexico. The authors thank Biokrone S. A. de C. V., Celaya, Guanajuato, Mexico, for providing the pesticides used in this work.

Funding

This study was financed by the Coordinación de la Investigación Científica, Universidad Michoacana de San Nicolás de Hidalgo.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Samuel Pineda.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morales, S.I., Martínez, A.M., Viñuela, E. et al. Parasitism, host feeding, and transgenerational effects of three insecticides on the eulophid parasitoid Tamarixia triozae when exposed in the immature stages. Environ Sci Pollut Res 27, 19473–19483 (2020). https://doi.org/10.1007/s11356-020-08475-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08475-z

Keywords

Navigation