Skip to main content

Advertisement

SpringerLink
Log in

Using multilevel models to explore the impact of abiotic and biotic conditions on the efficacy of pirimiphos-methyl against Tenebrio molitor L.

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

Abstract

In this study, we utilized a hierarchical multilevel modeling approach to test the hypothesis that the activity of the organophosphate insecticide pirimiphos-methyl against the cosmopolitan serious secondary pest of stored products, the yellow mealworm, Tenebrio molitor (Coleoptera: Tenebrionidae), is affected by temperature, relative humidity (RH), and developmental stage (adults, small larvae, large larvae). Our results showed that as temperature increased from 20 to 25 °C, the observed mortality of T. molitor was significantly higher. Furthermore, mortality at 25 °C did not significantly differ from that of 30 °C. An ultimate increase at 35 °C resulted in the highest mortality rate of T. molitor. However, an increase of RH from 55 to 75% adversely affected the efficacy of pirimiphos-methyl. In our study, it is also shown that the insect developmental stage is a critical feature of pirimiphos-methyl efficacy. Tenebrio molitor adults exhibited significantly higher mortality than larvae. In addition, small larvae showed significantly higher mortality than large larvae. Thus, adult is the most susceptible developmental stage of T. molitor to pirimiphos-methyl treatment. Our results could be useful tools for the management of T. molitor by indicating the optimum combination of temperature and RH that favors the insecticidal treatment against this species. In addition, we expect that the percentage of developmental stages in a whole population of T. molitor affects the insecticidal efficacy of pirimiphos-methyl.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adamski Z, Bufo SA, Chowański S, Falabella P, Lubawy J, Marciniak P, Pacholska Bogalska J, Salvia R, Scrano L, Słocińska M, Spochacz M, Szymczak M, Urbański A, Wałkowiak Nowicka K, Rosiński G (2019) Beetles as model organisms in physiological, biomedical and environmental sciences - a review. Front Physiol 10:319

    Article  Google Scholar 

  • Arthur FH, Subramanyam B (2012) Chemical control in stored products. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection. Kansas State University, Manhattan, pp 95–100

    Google Scholar 

  • Arthur FH, Yue B, Wilde GE (2004) Susceptibility of stored-product beetles on wheat and maize treated with thiamethoxam: effects of concentration, exposure interval, and temperature. J Stored Prod Res 40:527–546

    Article  CAS  Google Scholar 

  • Athanassiou CG, Kavallieratos NG, Vayias BJ, Panoussakis EC (2008) Influence of grain type on the susceptibility of different Sitophilus oryzae (L.) populations, obtained from different rearing media, to three diatomaceous earth formulations. J Stored Prod Res 44:279–287

    Article  CAS  Google Scholar 

  • Athanassiou CG, Kavallieratos NG, Boukouvala MC, Mavroforos ME, Kontodimas DC (2015) Efficacy of alpha-cypermethrin and thiamethoxam against Trogoderma granarium Everts (Coleoptera: Dermestidae) and Tenebrio molitor L. (Coleoptera: Tenebrionidae) on concrete. J Stored Prod Res 62:101–107

    Article  Google Scholar 

  • Athanassiou CG, Kavallieratos NG, Benelli G, Losic D, Usha Rani P, Desneux N (2018) Nanoparticles for pest control: current status and future perspectives. J Pest Sci 91:1–15

    Article  Google Scholar 

  • Attygalle AB, Blankespoor CL, Meinwald J, Eisner T (1991) Defensive secretion of Tenebrio molitor (Coleoptera: Tenebrionidae). J Chem Ecol 17:805–809

    Article  CAS  Google Scholar 

  • Bardini R, Politano G, Benso A, Di Carlo S (2017) Multi-level and hybrid modelling approaches for systems biology. Comp Struct Biotechnol J 15:396–402

    Article  CAS  Google Scholar 

  • Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1

    Article  Google Scholar 

  • Broekman HCHP, Verhoeckx KCM, Den Hartog JC, Kruizinga AG, Pronk Kleinjan M, Remington BC, Bruijnzeel Koomen CAFM, Houben GF, Knulst AC (2016) Majority of shrimp-allergic patients are allergic to mealworm. J Allergy Clin Immunol 137:1261–1263

    Article  Google Scholar 

  • Broekman HCHP, Knulst ACK, Den Hartog JC, Van Bilsen JHM, Raymakers FML, Kruizinga AG, Gaspari M, Gabriele C, Bruijnzeel Koomen CAFM, Houben GF, Verhoeckx KCM (2017) Primary respiratory and food allergy to mealworm. J Allergy Clin Immunol 140:600–603

    Article  Google Scholar 

  • Campbell JF, Arthur FH, Mullen MA (2004) Insect management in food processing facilities. In: Taylor S (ed) Advances in food and nutrition research, 48th edn. Elsevier, Amsterdam, pp 239–295

    Google Scholar 

  • Castilla AM, Dauwe T, Mora I, Malone J, Guitart R (2010) Nitrates and herbicides cause higher mortality than the traditional organic fertilizers on the grain beetle, Tenebrio molitor. Bull Environ Contam Toxicol 84:101–105

    Article  CAS  Google Scholar 

  • Crawley M (2013) The R book, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Cressie N, Calder C, Clark J, Hoef J, Wikle C (2009) Accounting for uncertainty in ecological analysis: the strengths and limitations of hierarchical statistical modeling. Ecol Appl 19:553–570

    Article  Google Scholar 

  • Deligeorgidis NP, Kavallieratos NG, Malesios C, Sidiropoulos G, Deligeorgidis PN, Benelli G, Papanikolaou NE (2019) Evaluation of combined treatment with mineral oil, fenoxycarb and chlorpyrifos against Cydia pomonella, Phyllonorycter blancardella and Synanthedon myopaeformis in apple orchards. Entomol Gen 39:117–126

    Article  Google Scholar 

  • Finke MD (2002) Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoobiology 21:269–285

    CAS  Google Scholar 

  • Garino C, Zagon J, Braeuning A (2019) Insects in food and feed - allergenicity risk assessment and analytical detection. EFSA J 17:e70907

    Google Scholar 

  • Hagstrum DW, Subramanyam B (2009) Stored-product insect resource. AACC International, St Paul

    Google Scholar 

  • Hamacher LS, Faroni LRD’A, Guedes RNC, Quieiróz MELR (2002) Persistence and activity towards Sitophilus zeamais (Coleoptera: Curculionidae) of pirimiphos-methyl sprayed at different temperatures on maize. J Stored Prod Res 38:167–175

    Article  CAS  Google Scholar 

  • Hill DS (2003) Pests of storage foodstuffs and their control. Kluwer Academic Publishers, New York

    Google Scholar 

  • Kavallieratos NG, Michail EJ, Boukouvala MC, Nika EP, Skourti A (2019) Efficacy of pirimiphos-methyl, deltamethrin, spinosad and silicoSec against adults and larvae of Tenebrio molitor L. on wheat, barley and maize. J Stored Prod Res 83:161–167

  • Kavallieratos NG, Boukouvala MC, Ntalli N, Kontodimas DC, Cappellacci L, Petrelli R, Ricciutelli M, Benelli G, Maggi F (2020) Efficacy of the furanosesquiterpene isofuranodiene against the stored-product insects Prostephanus truncatus (Coleoptera: Bostrychidae) and Trogoderma granarium (Coleoptera: Dermestidae). J Stored Prod Res 86:101553

    Article  Google Scholar 

  • Levy R (2012) Probabilistic models in the study of language. University of California, San Diego

    Google Scholar 

  • Messenger PS (1959) Bioclimatic studies with insects. Annu Rev Entomol 4:183–206

    Article  Google Scholar 

  • Meyling NV, Arthur S, Pedersen KE, Dhakal S, Cedergreen N, Fredensborg BL (2018) Implications of sequence and timing of exposure for synergy between the pyrethroid insecticide alpha-cypermethrin and the entomopathogenic fungus Beauveria bassiana. Pest Manag Sci 74:2488–2495

    Article  CAS  Google Scholar 

  • Mewis I, Ulrichs C (2001) Action of amorphous diatomaceous earth against different stages of the stored product pests Tribolium confusum, Tenebrio molitor, Sitophilus granarius and Plodia interpunctella. J Stored Prod Res 37:153–164

    Article  CAS  Google Scholar 

  • O’Donnell MJ (1980) The toxicities of four insecticides to Tribolium confusum Duv. in two sets of conditions of temperature and humidity. J Stored Prod Res 16:71–74

    Article  Google Scholar 

  • Papanikolaou NE, Kalaitzaki A, Karamaouna F, Michaelakis A, Papadimitriou V, Dourtogou V, Papachristos DP (2018) Nanoformulation enhances insecticidal activity against natural pyrethrins against Aphis gossypii (Hemiptera: Aphididae) and retains their harmless effect to non-target arthropods. Environ Sci Pollut Res 25:10243–10249

    Article  CAS  Google Scholar 

  • Papanikolaou NE, Kavallieratos NG, Kondakis N, Boukouvala MC, Nika EP, Demiris N (2019) Elucidating fitness components of the invasive dermestid beetle Trogoderma granarium Everts (Coleoptera: Dermestidae) at constant temperatures, combining deterministic and stochastic demography. PLoS One 14:e0212182

    Article  CAS  Google Scholar 

  • Park JB, Choi WH, Kim SH, Jin HJ, Han YS, Lee YS, Kim NJ (2014) Developmental characteristics of Tenebrio molitor larvae (Coleoptera: Tenebrionidae) in different instars. Int J Ind Entomol 28:5–9

    Google Scholar 

  • Plata Rueda A, Martínez LC, Dos Santos MH, Fernandes FL, Wilcken CF, Soares MA, Serrão JE (2017) Insecticidal activity of garlic essential oil and their constituents against the mealworm beetle, Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae). Sci Rep 7:46406

    Article  CAS  Google Scholar 

  • Pozidi Metaxa E, Athanassiou CG (2013) Comparison of spinosad with three traditional grain protectants against Prostephanus truncatus (Horn) and Ephestia kuehniella (Zeller) at different temperatures. J Pest Sci 86:203–209

    Article  Google Scholar 

  • Punzo F, Mutchmor JA (1980) Effects of temperature, relative humidity and period of exposure on the survival capacity of Tenebrio molitor (Coleoptera: Tenebrionidae). J Kansas Entomol Soc 53:260–270

    Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna. http://www.r-project.org. Accessed 27 Aug 2018

  • Raudenbush SW, Bryk AS (2002) Hierarchical linear models. Applications and data analysis methods. In: Advanced Quantitative Techniques in the Social Sciences, Series 1 edn. Sage Publications, Inc, Thousand Oaks

    Google Scholar 

  • Robinson WH (2005) Urban insects and arachnids. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rees D (2004) Insects of stored products. Manson Publishing, London

    Book  Google Scholar 

  • Rumbos CI, Dutton AC, Athanassiou CG (2013) Comparison of two pirimiphos-methyl formulations against major stored-product insect species. J Stored Prod Res 55:106–115

    Article  Google Scholar 

  • Skourti A, Kavallieratos NG, Papanikolaou NE (2019) Laboratory evaluation of development and survival of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) under constant temperatures. J Stored Prod Res 83:305–310

    Article  Google Scholar 

  • Smith LW Jr, Pratt JJ Jr, Nii I, Umina AP (1971) Baking and taste properties of bread made from hard wheat flour infested with species of Tribolium, Tenebrio, Trogoderma and Oryzaephilus. J Stored Prod Res 6:307–316

    Article  Google Scholar 

  • Trewin B, Reichmuth C (1997) Wirksamkeit des kieselgurpräparates Dryacide® gegen vorratsschädliche Insekten. Anz Schädlingsk Pflanzen Umweltschutz 70:51–54

    Article  Google Scholar 

  • Tschinkel WR (1975) A comparative study of the chemical defensive system of tenebrionid beetles. J Morphol 145:355–370

    Article  Google Scholar 

  • Vayias BJ, Athanassiou CG (2004) Factors affecting the insecticidal efficacy of the diatomaceous earth formulation SilicoSec adults and larvae of the confused flour beetle, Tribolium confusum DuVal (Coleoptera: Tenebrionidae). Crop Prot 23:565–573

    Article  CAS  Google Scholar 

  • Veldkamp T, Van Duinkerken G, Van Huis A, Lakemond CMM, Ottevanger E, Bosch G, Van Boekel MAJS (2012) Insects as a sustainable feed ingredient in pig and poultry diets - a feasibility study. In: Report 638. Wageningen UR Livestock Research, Lelystad, pp 3–10

    Google Scholar 

  • Verhoeckx KCM, Van Broekhoven S, Den Hartog JC, Gaspari M, De Jong GAH, Wichers HJ, Van Hoffen E, Houben GF, Knulst AC (2014) House dust mite (Der p 10) and crustacean allergic patients may react to food containing yellow mealworm proteins. Food Chem Toxicol 65:364–373

    Article  CAS  Google Scholar 

  • Vigneron A, Jehan C, Rigaud T, Moret Y (2019) Immune defenses of a beneficial pest: the mealworm beetle, Tenebrio molitor. Front Physiol 10:138

    Article  Google Scholar 

Download references

Funding

This study was partially funded by the 34.0401 project (Special Account for Research Funds of the Agricultural University of Athens).

Author information

Authors and Affiliations

  1. Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, 75 Iera Odos Str., 11855, Athens, Attica, Greece

    Nickolas G. Kavallieratos, Nikos E. Papanikolaou, Andriana N. Kazani & Maria C. Boukouvala

  2. Directorate of Plant Produce Protection, Greek Ministry of Rural Development and Food, 150 Sygrou Avenue, 17671, Athens, Attica, Greece

    Nikos E. Papanikolaou

  3. Department of Agricultural Economics and Rural Development, Agricultural University of Athens, 75 Iera Odos str, 11855, Athens, Attica, Greece

    Chrisovalantis Malesios

Authors
  1. Nickolas G. Kavallieratos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikos E. Papanikolaou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andriana N. Kazani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria C. Boukouvala
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chrisovalantis Malesios
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NGK conceived, designed, and supervised the research. AK conducted experiments. MCB curated the data. NEP and CM analyzed the data. NGK, NEP, MCB, and CM drafted the manuscript. All authors revised the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Nikos E. Papanikolaou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

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

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Responsible Editor: Philippe Garrigues

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

Kavallieratos, N.G., Papanikolaou, N.E., Kazani, A.N. et al. Using multilevel models to explore the impact of abiotic and biotic conditions on the efficacy of pirimiphos-methyl against Tenebrio molitor L.. Environ Sci Pollut Res 28, 17200–17207 (2021). https://doi.org/10.1007/s11356-020-11925-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-11925-3

Keywords

Search

Navigation