Skip to main content
SpringerLink
Log in

Acute toxicity of the insecticide abamectin and the fungicide difenoconazole (individually and in mixture) to the tropical stingless bee Melipona scutellaris

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Stingless bees have been recognized as essential plant pollinators and producers of various natural products in neotropical areas. Research into the potential risks of pesticides they may be exposed to in agricultural fields, however, remains meagre. Especially the toxicity of pesticide mixtures likely to occur under real-world conditions and that are likely to exert synergetic effects has been poorly studied. The aim of the present study was therefore to evaluate the single and mixture acute contact and oral toxicity of commercial products containing the insecticide abamectin and the fungicide difenoconazole in laboratory bioassays with the Brazilian native stingless bee Melipona scutellaris. In addition, a comparison of the insecticide sensitivity of stingless bees relative to the honeybee Apis mellifera was made based on previously published toxicity data. Except for oral exposure to abamectin, M. scutellaris appeared to be more sensitive that A. mellifera in the single compound toxicity tests. A difenoconazole concentration at the NOEC (no observed effect concentration) level indicated a synergetic toxic interaction with abamectin. A sensitivity comparison based on published toxicity data for A. mellifera and stingless bees indicated several insecticidal modes of action having a high relative sensitivity to stingless bees that need especial consideration in future studies. The research findings highlight the need for testing native bee species and environmentally relevant pesticide mixtures in risk assessments to avoid underestimation of potential risks to bee populations and the subsequent loss of pollination ecosystem services.

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

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this manuscript. Raw data are available from the corresponding author upon request (m.daam@fct.unl.pt).

References

  • Almasri H, Tavares DA, Pioz M, Sené D, Tchamitchian S, Cousin M, Brunet JL, Belzunces LP (2020) Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicol Environ Saf 203:111013. https://doi.org/10.1016/j.ecoenv.2020.111013

    Article  CAS  Google Scholar 

  • Araújo RS, Bernardes RC, Martins GF (2021) A mixture containing the herbicides Mesotrione and Atrazine imposes toxicological risks on workers of Partamona helleri. Sci Total Environ 763:142980. https://doi.org/10.1016/j.scitotenv.2020.142980

    Article  CAS  Google Scholar 

  • Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:324–334. https://doi.org/10.1007/s10646-014-1190-1

    Article  CAS  Google Scholar 

  • Barbosa WF, Smagghe G, Guedes RNC (2015) Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest Manag Sci 71:1049–1053. https://doi.org/10.1002/ps.4025

    Article  CAS  Google Scholar 

  • Bernardes RC, Barbosa WF, Martins GF, Lima MAP (2018) The reduced-risk insecticide azadirachtin poses a toxicological hazard to stingless bee Partamona helleri (Friese, 1900) queens. Chemosphere 201:550–556. https://doi.org/10.1016/j.chemosphere.2018.03.030

    Article  CAS  Google Scholar 

  • Cham KO, Nocelli RCF, Borges LO, Viana-Silva FEC, Tonelli CAM, Malaspina O, Menezes C, Rosa-Fontana AS, Blochtein B, Freitas BM, Pires CSS, Oliveira FF, Contrera FAL, Torezani KRS, Ribeiro MF, Siqueira MAL, Rocha MCLSA (2019) Pesticide exposure assessment paradigm for stingless bees. Environ Entomol 48:36–48. https://doi.org/10.1093/ee/nvy137

    Article  Google Scholar 

  • de Figueirêdo LP, Athayde DB, Daam MA, van Gestel CAM, Guerra GS, Duarte-Neto PJ, Espíndola ELG (2020) Impact of temperature on the toxicity of Kraft 36 EC® (a.s. abamectin) and Score 250 EC® (a.s. difenoconazole) to soil organisms under realistic environmental exposure scenarios. Ecotoxicol Environ Saf 194:110446. https://doi.org/10.1016/j.ecoenv.2020.110446

    Article  CAS  Google Scholar 

  • de Morais CR, Travençolo BAN, Carvalho SM, Beletti ME, Santos VSV, Campos CF, Júnior EOC, Pereira BB, Naves MPC, de Rezende AAA, Spanó MA, Vieira CU, Bonetti AM (2018) Ecotoxicological effects of the insecticide fipronil in Brazilian native stingless bees Melipona scutellaris (Apidae: Meliponini). Chemosphere 206:632–642. https://doi.org/10.1016/j.chemosphere.2018.04.153

    Article  CAS  Google Scholar 

  • de Oliveira RC, Queiroz SCN, da Luz CFP, Porto RS, Rath S (2016) Bee pollen as a bioindicator of environmental pesticide contamination. Chemosphere 163:525–534. https://doi.org/10.1016/j.chemosphere.2016.08.022

    Article  CAS  Google Scholar 

  • Del Sarto MCL, Oliveira EE, Guedes RNC, Campos LAO (2014) Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honeybee Apis mellifera. Apidologie 45:626–636. https://doi.org/10.1007/s13592-014-0281-6

    Article  CAS  Google Scholar 

  • Devillers J, Devillers H (2020) Lethal and sublethal effects of pyriproxyfen on Apis and non-Apis bees. Toxics 8:104. https://doi.org/10.3390/toxics8040104

    Article  CAS  Google Scholar 

  • do Prado FSR, dos Santos DM, Oliveira TMA, Burgarelli JAM, Castele JB, Vieira EM (2020) Determination and uptake of abamectin and difenoconazole in the stingless bee Melipona scutellaris Latreille, 1811 via oral and topic acute exposure. Environ. Pollut. 265:114313. https://doi.org/10.1016/j.envpol.2020.114313

    Article  CAS  Google Scholar 

  • Dorigo AS, Rosa-Fontana AS, Camargo IF, Nocelli RCF, Malaspin O (2018) Biological data of stingless bees with potential application in pesticide risk assessments. Sociobiology 65:777–779

    Article  Google Scholar 

  • Dorneles AL, Souza Rosa A, Blochtein B (2017) Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi. Apidologie 48:612–620. https://doi.org/10.1007/s13592-017-0502-x

    Article  CAS  Google Scholar 

  • EC (2006a) Draft Assessment Report (DAR) – Public version – Initial risk assessment provided by the Rapporteur Member State Sweden for the existing active substance difenoconazole of the third stage (Part A) of the review programme referred to in Article 8(2) of Council Directive 91/414/EEC

  • EC (2006b) Draft Assessment Report (DAR) – Public version – Initial risk assessment provided by the Rapporteur Member State the Netherlands for the existing active substance abamectin of the third stage (Part A) of the review programme referred to in Article 8(2) of Council Directive 91/414/EEC

  • EFSA (2013) EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11:3295

    Google Scholar 

  • EFSA (2020) Peer review of the pesticide risk assessment of the active substance abamectin. EFSA J 18:e06227. https://doi.org/10.2903/j.efsa.2020.6227

    Article  CAS  Google Scholar 

  • FAO (2014) Pollinator safety in agriculture. Food and agriculture organization of the United nations. http://www.fao.org/3/a-i3800e.pdf

  • FRAC (2020) FRAC Code List 2020: Fungal control agents sorted by cross resistance pattern and mode of action (including FRAC Code numbering). Fungicide Resistance Action Committee (FRAC). Available via: https://www.frac.info/docs/default-source/publications/frac-code-list/frac-code-list-2020-final.pdf?sfvrsn=8301499a_2

  • Gregorc A, Alburaki M, Rinderer N, Sampson B, Knight PR, Karim S, Adamczyk J (2018) Effects of coumaphos and imidacloprid on honeybee (Hymenoptera: Apidae) lifespan and antioxidant gene regulations in laboratory experiments. Sci Rep 8:15003. https://doi.org/10.1038/s41598-018-33348-4

    Article  CAS  Google Scholar 

  • Grüter C (2020) Stingless bees—Their behaviour, ecology and evolution. Springer, Switzerland

    Book  Google Scholar 

  • Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, fungicide and drug interactions in honeybees (Apis mellifera). PLoS ONE 8:e54092. https://doi.org/10.1371/journal.pone.0054092

    Article  CAS  Google Scholar 

  • Ladurner E, Bosch J, Kemp WP, Maini S (2005) Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and Apis mellifera. Apidologie 36:449–460. https://doi.org/10.1051/apido:2005032

    Article  CAS  Google Scholar 

  • Lima MAP, Martins GF, Oliveira EE, Guedes RNC (2016) Agrochemical‐induced stress in stingless bees: peculiarities, underlying basis, and challenges. J Comp Physiol A 202:733–747. https://doi.org/10.1007/s00359-016-1110-3

    Article  CAS  Google Scholar 

  • MAPA – Ministério da Agricultura, Pecuária e Abastecimento 2021. Agrofit, Sistemas de Agrotóxicos Fitossanitários. Freely accessible via: http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons (Accessed 20 February 2021)

  • Marletto F, Patetta A, Manino A (2003) Laboratory assessment of pesticide toxicity to bumblebees. Bull Insectology 56:155–158

    Google Scholar 

  • Moreira RA, de Araujo GS, Silva ARRG, Daam AM, Rocha O, Soares AMVM, Loureiro S (2020) Effects of abamectin-based and difenoconazole-based formulations and their mixtures in Daphnia magna: a multiple endpoint approach. Ecotoxicology 29:1486–1499

    Article  CAS  Google Scholar 

  • Moreira DR, Gigliolli AAS, Falco JRP, Julio AHF, Volnistem EA, Chagas F, Toledo VAA, Ruvolo-Takasusuki MCC (2018) Toxicity and effects of the neonicotinoid thiamethoxam on Scaptotrigona bipunctata lepeletier, 1836 (Hymenoptera: Apidae). Environ Toxicol 33:463–475. https://doi.org/10.1002/tox.22533

    Article  CAS  Google Scholar 

  • Moreno SC, Silvério FO, Lopes MC, Ramos RS, Alvarenga ES, Picanço MC (2017) Toxicity of new pyrethroid in pest insects Asciamonuste and Diaphania hyalinata, predator Solenopsis saevissima and stingless bee Tetragonisca angustula. J Environ Sci Health B 52:237–243. https://doi.org/10.1080/03601234.2016.1270681

    Article  CAS  Google Scholar 

  • Novelli A, Vieira BH, Braun AS, Mendes LB, Daam MA, Espíndola ELG (2016) Impact of runoff water from an experimental agricultural field applied with Vertimec® 18EC (abamectin) on the survival, growth and gill morphology of zebrafish juveniles. Chemosphere 144:1408–1414. https://doi.org/10.1016/j.chemosphere.2015.10.004

    Article  CAS  Google Scholar 

  • OECD (1998a) Honeybees, acute contact toxicity test. Guideline for Testing Chemicals No. 214. Organisation for Economic Co-operation and Development, Paris, France

    Book  Google Scholar 

  • OECD (1998b) Honeybees, acute oral toxicity test. Guideline for Testing Chemicals No. 213. Organisation for Economic Co-operation and Development, Paris, France

    Book  Google Scholar 

  • OECD (2017a) Bumblebee, acute contact toxicity test. Guideline for Testing Chemicals No. 246. Organisation for Economic Co-operation and Development, Paris, France

    Book  Google Scholar 

  • OECD (2017b) Bumblebee, acute oral toxicity test. Guideline for Testing Chemicals No. 247. Organisation for Economic Co-operation and Development, Paris, France

    Book  Google Scholar 

  • Piovesan B, Padilha AC, Morais MC, Botton M, Grützmacher AD, Zotti MJ (2020) Effects of insecticides used in strawberries on stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi (Hymenoptera: Apidae). Environ Sci Pollut Res 27:42472–42480. https://doi.org/10.1007/s11356-020-10191-7

    Article  CAS  Google Scholar 

  • Roessink I, Van der Steen JJM, Kasina M, Gikungu M, Nocelli RCF (2011) Is the European honeybee (Apis mellifera) a good representative for other pollinator species? SETAC Europe 21st Annual Meeting, Milan, Italy

  • Sánchez-Bayo F, Goka K (2014) Pesticide residues and bees – A risk assessment. PLoS ONE 9:e94482. https://doi.org/10.1371/journal.pone.0094482

    Article  CAS  Google Scholar 

  • Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020

    Article  Google Scholar 

  • Seide VE, Bernardes RC, Pereira EJG, Lima MAP (2018) Glyphosate is lethal and Cry toxins alter the development of the stingless bee Melipona quadrifasciata. Environ Pollut 243:1854–1860. https://doi.org/10.1016/j.envpol.2018.10.020

    Article  CAS  Google Scholar 

  • Sgolastra F, Medrzycki P, Bortolotti L, Maini S, Porrini C, Simon-Delso N, Bosch J (2020) Bees and pesticide regulation: Lessons from the neonicotinoid experience. Biol Conserv 241:108356. https://doi.org/10.1016/j.biocon.2019.108356

    Article  Google Scholar 

  • Statsoft (2004) Statistica version 07. Freely accessible via www.statsoft.com

  • Straub L, Williams GR, Vidondo B, Khongphinitbunjong K, Retschnig G, Schneeberger A, Chantawannakul P, Dietemann V, Neumann P (2019) Neonicotinoids and ectoparasitic mites synergistically impact honeybees. Sci Rep 9:8159. https://doi.org/10.1038/s41598-019-44207-1

    Article  CAS  Google Scholar 

  • Systat (2008) Systat Software, Incorporation SigmaPlot for Windows Version 11.0

  • Tomé HVV, Ramos GS, Araújo MF, Santana WC, Santos GR, Guedes RNC, Maciel CD, Newland PL, Oliveira EE (2017) Agrochemical synergism imposes higher risk to Neotropical bees than to honeybees. R Soc open sci 4:160866. 10.1098%2Frsos.160866

    Article  CAS  Google Scholar 

  • Van Vlaardingen P, Traas TP, Wintersen AM, Aldenberg T (2004) ETX 2.0. A program to calculate hazardous concentrations and fraction affected, based on normally distributed toxicity data. RIVM report no. 601501028/2004, Bilthoven, The Netherlands

    Google Scholar 

  • Vandame R, Belzunces LP (1998) Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neurosci Lett 251:57–60. https://doi.org/10.1016/S0304-3940(98)00494-7

    Article  CAS  Google Scholar 

  • Viana-Silva F, Pires C, Torezani K, Borges L, Cham K, Dias C, Teixeira I, Tonelli C, Belchior C, Marcondes C, Nocelli R, Malaspina O, Cione A, Shiwa A, Ferraz A (2018) 1.12 Selection matrix for Brazilian bee species to risk assessment of pesticides. Julius-Kühn-Archiv 462:56–61

    Google Scholar 

  • Wogram J, Liess M (2001) Rank ordering of macroinvertebrate species sensitivity to toxic compounds by comparison with that of Daphnia magna. Bull Environ Contam Toxicol 67:360–367. https://doi.org/10.1007/s001280133

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the Brazilian Foundation for Research Support of the State of São Paulo (FAPESP 2018/16244-0). Financial support was also provided to M. Daam by the Portuguese government (Fundação para a Ciência e Tecnologia; FCT) through the research unit UIDB/04085/2020 (CENSE).

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by JB and JOC. The first draft of the manuscript was written by JB and MAD and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. NEEA/CRHEA/SHS, São Carlos Engineering School, University of São Paulo, Av. Trabalhador São Carlense, 400, São Carlos, 13.560-970, Brazil

    Janete Brigante, Joyce Oliveira Costa & Evaldo L. G. Espíndola

  2. CENSE, Department of Environmental Sciences and Engineering, Faculty of Sciences and Technology, New University of Lisbon, Quinta da Torre, 2829-516, Caparica, Portugal

    Michiel A. Daam

Authors
  1. Janete Brigante
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joyce Oliveira Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Evaldo L. G. Espíndola
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michiel A. Daam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michiel A. Daam.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

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

Brigante, J., Costa, J.O., Espíndola, E.L.G. et al. Acute toxicity of the insecticide abamectin and the fungicide difenoconazole (individually and in mixture) to the tropical stingless bee Melipona scutellaris. Ecotoxicology 30, 1872–1879 (2021). https://doi.org/10.1007/s10646-021-02458-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-021-02458-7

Keywords

Search

Navigation