Skip to main content

Life history study of the mirid Tupiocoris cucurbitaceus feeding on Tuta absoluta eggs: implications for biological control and its combination with inherited sterility

Abstract

Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a key pest of tomato crops. Tupiocoris cucurbitaceus (Spinola) (Hemiptera: Miridae) is a neotropical predator capable of consuming T. absoluta eggs. We evaluated the life history traits of T. cucurbitaceus on three different diets: T. absoluta eggs from irradiated parental males and untreated parents, and Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae) eggs (control). The nymphal development of T. cucurbitaceus was reached in 13 days with a similar survival for all diets (58–65%). Mirid female longevity and oviposition period were statistically similar when the diets consisted of T. absoluta eggs from untreated parents and S. cerealella eggs, although the number of nymphs laid was larger with the second diet. Moreover, mirid females feeding on T. absoluta eggs from untreated parents lived longer and laid double number of nymphs than when fed on T. absoluta eggs from irradiated parental males. The highest intrinsic rate of increase (rm) was observed for the S. cerealella eggs diet, while differences were not observed between the two types of T. absoluta eggs. These results indicate that the mirid could develop and reproduce by feeding exclusively on both types of T. absoluta eggs. As conclusion, the use of more environmentally friendly strategies to control this pest, such as the biological control and inherited sterility, is possible through the release of T. cucurbitaceus and irradiated T. absoluta individuals.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Data availability

The data will be available upon request from corresponding author.

References

  • Agustí N, Gabarra R (2009) Puesta a punto de una cría masiva del depredador polífago Dicyphus tamanii Wagner (Hemiptera: Miridae). Bol San Veg Plagas 35:205–218

    Google Scholar 

  • Arnó J, Sorribas R, Prat M, Matas M, Pozo C, Rodríguez D, Garreta A, Gómez A, Gabarra R (2009) Tuta absoluta, a new pest in IPM tomatoes in the northeast of Spain. IOBC/WPRS Bulletin 9:203–208

    Google Scholar 

  • Arnó J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present and future. Annu Rev Entomol 63:239–258

    CAS  Article  Google Scholar 

  • Bloem S, Bloem KA (2000) SIT for codling moth eradication in British Columbia, Canada. In: Tan KH (ed) Area-wide control of fruit flies and other insect pest. Penerbirt University Sains Malaysia, Pulau Pinang, Malaysia, pp 207–214

    Google Scholar 

  • Cagnotti CL, Viscarret MM, Riquelme MB, Botto EN, Carabajal LZ, Segura DF, López SN (2012) Effects of X rays on Tuta absoluta (Lepidoptera: Gelechiidae) for use in inherited sterility programmes. J Pest Sci 85:413–421

    Article  Google Scholar 

  • Campos M, Biondi A, Adiga A, Guedes RN, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90:787–796

    Article  Google Scholar 

  • Carabajal Paladino LZ, Ferrari ME, Lauría JP, Cagnotti CL, Síchová J, López SN (2016) The effect of X-rays on cytological traits of Tuta absoluta (Lepidoptera: Gelechiidae). Fla entomol 99:43–53

    Article  Google Scholar 

  • Carpenter JE, Bloem S, Marec F (2005) Inherited sterility in insects. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile Insect Technique. Springer, The Netherlands, pp 115–146

    Chapter  Google Scholar 

  • Chinchilla-Ramírez M, Garzo E, Fereres A, GavaraVidal J, Broeke CJM, van Loon JJA, Urbaneja A, Pérez-Hedo M (2021) Plant feeding by Nesidiocoris tenuis: quantifying its behavioral and mechanical components. Biol Control. https://doi.org/10.1016/j.biocontrol.2020.104402

    Article  Google Scholar 

  • de Coelho MCF, Franca FH (1987) Biologia, quetotaxia da larva e descricao da pupa e adulto da traca-do-tomateiro. Pesqui Agropecu Bras 22:129–135

    Google Scholar 

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

    CAS  Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Drummond BA (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, London, United Kingdom, pp 291–370

    Chapter  Google Scholar 

  • Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25:140–146

    Article  Google Scholar 

  • Friedlanänder M (1997) Control of the eupyrene-apyrene sperm dimorphism in the Lepidoptera. J Insect Physiol 43:1085–1092

    Article  Google Scholar 

  • Friedlanänder M, Hauschteck-Jungen E (1982) Differential basic nucleoprotein kinetics in the two kinds of Lepidoptera spermatids: nucleate (eupyrene) and anucleate (apyrene). Chromosoma 85:387–398

    Article  Google Scholar 

  • Guedes RNC, PicanÇo MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216

    Article  Google Scholar 

  • Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252

    Article  Google Scholar 

  • Karr T, Walters J (2015) Panning for sperm gold: isolation and purification of apyrene and eupyrene sperm from lepidopterans. Insect Biochem Mol Biol 63:152–158

    CAS  Article  Google Scholar 

  • Knipling EF (1964) The potential role of the sterility method for insect population control with special reference to combining this method with conventional methods. Serie 33-98. USDA/ARS, Washington, DC, USA

  • Knipling EF (1992) Principles of insect parasitism analyzed from new perspectives: practical implications for regulating insect populations by biological means. Agricultural handbook vol 693, USDA ARS, Washington, DC, p 337

  • LaChance LE (1985) Genetic methods for the control of the lepidopteran species: status and potential. US Department of Agriculture, Washington, DC

    Book  Google Scholar 

  • La Rossa FR (2015) Nuevo programa informático para la construcción de tablas de vida y la estimación de parámetros biológicos y poblacionales en insectos. In: Libro de resúmenes IX Congreso Argentino de Entomología. Posadas, Misiones, Argentina, 19-22 mayo 2015. p 281

  • López SN, Arce Rojas F, Villalba Velasquez V, Cagnotti C (2012) Biology of Tupiocoris cucurbitaceus (Hemiptera: Miridae), a predator of the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) in tomato crops in Argentina. Biocontrol Sci Technol 22:1107–1117

    Article  Google Scholar 

  • López SN, Orozco Muñoz A, Andorno AV, Cuello EM, Cagnotti CL (2019) Predatory capacity of Tupiocoris cucurbitaceus (Hemiptera: Miridae) on several pests of tomato. Bull Insectol 72:201–205

    Google Scholar 

  • Mancini K, Dolder H (2004) Protein detection spermatids and spermatozoa of the butterfly Euptoieta hegesia (Lepidoptera). Biocell 28:299–310

    CAS  Article  Google Scholar 

  • Ministerio de Agroindustria (2017) Mercado externo del tomate. https://www.magyp.gob.ar/sitio/areas/ss_mercados_agropecuarios/areas/hortalizas/_archivos/000030_Informes/000994_Informe%20del%20Mercado%20Externo%20del%20Tomate%20-%202017.pdf. Accessed 14 May 2020

  • Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl 59:175–183

    Article  Google Scholar 

  • Nagel P, Peveling R (2005) Environment and the Sterile Insect Technique. Chapter 5.2. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile Insect Technique. Springer, The Netherlands, pp 429–524

    Google Scholar 

  • North DT (1975) Inherited sterility in Lepidoptera. Annu Rev Entomol 20:167–182

    CAS  Article  Google Scholar 

  • Orozco Muñoz A, Villalba Velásquez V, López SN (2012) Desarrollo de Tupiocoris cucurbitaceus Spinola (Hemiptera: Miridae) sobre Bemisia tabaci (Hemiptera: Aleyrodidae) en diversas hortalizas. Fitosanidad 16:147–153

    Google Scholar 

  • Osanai M, Kasuga H, Aigaki T (1989) Isolaton of eupyrene sperm bundles and apyrene spermatozoa from seminal fluid of the silkmoth, Bombyx mori. J Insect Physiol 35:401–408

    CAS  Article  Google Scholar 

  • Polack LA, López SN, Silvestre C, Viscarret MM, Andorno AV, del Pino M, Peruzzi G, Gómez J, Iezzi A (2017) Control biológico en tomate con el mírido Tupiocoris cucurbitaceus. Instituto Nacional de Tecnología Agropecuaria (INTA). https://inta.gob.ar/documentos/control-biologico-en-tomate-con-el-mirido-tupiocoris-cucurbitaceus Accessed 14 May 2020

  • Salas Gervassio NG, Aquino DA, Vallina C, Biondi A, Luna MG (2019) A re-examination of Tuta absoluta parasitoids in South America for optimized biological control. J Pest Sci 92:1343–1357

    Article  Google Scholar 

  • Santana PA, Kumar L, Da Silva RS, Picanco MC, (2018) Global geographic distribution of Tuta absoluta as affected by climate change. J Pest Sci 92:1373–1385

    Article  Google Scholar 

  • Silva JE, Assis CP, Ribeiro LM, Siqueira HA (2016) Field-evolved resistance and cross-resistance of brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195

    CAS  Article  Google Scholar 

  • Silva DB, Bueno VHP, Montes FC, van Lenteren JC (2016) Population growth of three mirid predatory bugs feeding on eggs and larvae of Tuta absoluta on tomato. BioControl 61:545–553

    Article  Google Scholar 

  • StatSoft (2000) Statistica for Windows. Computer program manual. StatSoft Inc., Tulsa, USA

  • Tonnang HEZ, Mohamed SF, Khamis F, Ekesi S (2015) Identification and risk assessment for worldwide invasion and spread of Tuta absoluta with a focus on Sub-Saharan Africa: implications for phytosanitary measures and management. PLoS ONE 10(8):e0135283

    Article  Google Scholar 

  • van Lenteren JC, Hemerik L, Lins JC, Bueno VHP (2016) Functional responses of three neotropical mirid predators to eggs of Tuta absoluta on tomato. Insects 7:34–44

    Article  Google Scholar 

  • van Lenteren JC, Bueno VHP, Smit J, Soares MA, Calixto AM, Montes FC, de Jong P (2017) Predation of Tuta absoluta eggs during the nymphal stages of three Neotropical mirid predators on tomato. Bull Insectol 70:69–74

    Google Scholar 

Download references

Acknowledgements

We thank Ana María López for helpful comments on an earlier version of our manuscript. We also thank Carmen Hernández and Diana Arias for technical support and the Instituto de Genética INTA for assistance with the radiation treatment using the X-Ray machine. This investigation received financial support from IAEA (International Atomic Energy Agency) and from Proyecto INTA PE-E4-I074-001.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cynthia L. Cagnotti.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or vertebrate animals performed by any of the authors.

Additional information

Handling Editor: Eric Riddick.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cagnotti, C.L., Arias, A.E., Ermantraut, E. et al. Life history study of the mirid Tupiocoris cucurbitaceus feeding on Tuta absoluta eggs: implications for biological control and its combination with inherited sterility. BioControl 66, 207–216 (2021). https://doi.org/10.1007/s10526-020-10054-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-020-10054-7

Keywords

  • Tuta absoluta
  • Tupiocoris cucurbitaceus
  • Biological control
  • Inherited sterility