Skip to main content
SpringerLink
Log in

Effects of insecticides used in strawberries on stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi (Hymenoptera: Apidae)

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

Abstract

The use of pesticides is considered one of the most important threats to pollinators, especially since they are widely used in agriculture for pest control. In the last years, several studies have reported severe secondary effects on various bee species, including exotic and native bees. In this study, lethal (mortality) and sublethal (locomotor activity) effects of insecticides and acaricides used in strawberries in Brazil (abamectin, novaluron, spinetoram, and thiamethoxam) were evaluated on the native stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi. The results showed that the effects varied significantly according to the pesticide, type of exposure (oral or topical), and bee species. Through oral exposure, M. quadrifasciata was more susceptible to all insecticides except for abamectin, while in topical exposure, T. fiebrigi was more sensitive. Thiamethoxam followed by spinetoram and abamectin were the most lethal, regardless of species or exposure route; novaluron was not harmful at the highest tested dose. The locomotor activity of bees was altered in the presence of sublethal doses (LC10 and LC50) of all insecticides. Spinetoram and abamectin can be as much as toxic as thiamethoxam against M. quadrifasciata and T. fiebrigi in laboratory experiments. These findings should be confirmed in field experiments to define possibilities to combine pest control and pollinator management. In crops like strawberries, the selectivity of native pollinators should be considered.

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

Similar content being viewed by others

References

  • (AGROFIT) Ministério da Agricultura Pecuária e Abastecimento (2019) Available in: <http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons>

  • (IRAC) Insecticide Resistance Action Committee (2020) Available in: <http: https://www.irac-br.org/folhetos>

  • (OECD) Organization for Economic Co-operation and Development (1998a) Guidelines for the testing of chemicals: honeybees, acute oral toxicity test. Environmental health safety division, organization for economic co-operation and development- Number 213, Paris, France

  • (OECD) Organization for Economic Co-Operation and Development (1998b) Guidelines for the testing of chemicals: honeybees, acute contact toxicity test. Environmental health safety division, organization for economic co-operation and development - Number 214, Paris, France

  • Aljedani DM (2017) Effects of Abamectin and Deltamethrin to the foragers honeybee workers of Apis mellifera jemenatica (Hymenoptera: Apidae) under laboratory conditions. Saudi J Biol Sci 24:1007–1015

    CAS  Google Scholar 

  • Antunes OT, Calvete EO, Rocha HC, Nienow AA, Cecchetti D, Riva E, Maran RE (2007) Produção de cultivares de morangueiro polinizadas pela abelha jataí em ambiente protegido. Hortic Bras 25:94–99

    Google Scholar 

  • Bacci L, Pereira EJG, Crespo ALB, Picanço MC, Coutinho DC, Sena ME (2007) Eficiência e seletividade de inseticidas para o manejo de mosca branca e inimigos naturais em melancia. Revista Ceres 54:47–54

    CAS  Google Scholar 

  • Bernardi D, Botton M, Nava DE, Zawadneak MAC (2015) Guia para a identificação e monitoramento de pragas e seus inimigos naturais em morangueiro. Embrapa, Brasília

    Google Scholar 

  • Biddinger DJ, Robertson JL, Mullin C, Frazier J, Ashcraft SA, Rajotte EG, Joshi NK, Vaughn M (2013) Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One 8:e72587

    CAS  Google Scholar 

  • Bortolotti L, Montanari R, Marcelino J, Mdrzycki P, Maini S, Porrini C (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull. Insectology 56:63–67

    Google Scholar 

  • Brito P, Elias M, Silva-Neto C, Sujii E, Silva D, Gonçalves B, Franceschinelli E (2020) The effects of field-realistic doses of imidacloprid on Melipona quadrifasciata (Apidae: Meliponini) workers. Environ Sci Pollut Res 1:1–8

    Google Scholar 

  • Brittain C, Potts SG (2011) The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl Ecol 12:321–331

    Google Scholar 

  • Brown LA, Ihara M, Buckingham SD, Matsuda K, Sattelle DB (2006) Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J Neurochem 99:608–615

    CAS  Google Scholar 

  • Camargo JMF, Pedro SRM (2013) Meliponini Lepeletier, 1836. In Moure JS, urban D, Melo GAR (orgs). Catalogue of bees (Hymenoptera, Apoidea) in the neotropical region - online version. Available at <http://www.moure.cria.org.br/catalogue>. Accessed 28 November 2017

  • Chagnon M, Gingras J, Oliveira D (1993) Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera). J Econ Entomol 86:416–420

    Google Scholar 

  • Charreton M, Decourtye A, Henry M, Rodet G, Sandoz JC, Charnet P, Collet C (2015) A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honeybee Apis mellifera. PLoS One 10:e0144879

    Google Scholar 

  • Christen V, Mittner F, Fent K (2016) Molecular effects of neonicotinoids in honey bees (Apis mellifera). Environ Sci Technol 50:4071–4081

    CAS  Google Scholar 

  • Costa EM, Araujo EL, Maia AVP, Silva FEL, Bezerra CES, Silva JG (2014) Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie 45:34–44

    CAS  Google Scholar 

  • Costa L, Grella MTC, Barbosa RA, Malaspina O, Nocelli RCF (2015) Determination of acute lethal doses (LD50 and LC50) of imidacloprid for the native bee Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae). Sociobiology 62:578–582

    Google Scholar 

  • Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157

    CAS  Google Scholar 

  • Decourtye A, Henry M, Desneux N (2013) Overhaul pesticide testing on bees. Nature 497:188

    CAS  Google Scholar 

  • Del Sarto MCL, Peruquetti RC, Campos LA (2005) Evaluation of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae) as pollinator of greenhouse tomatoes. J Econ Entomol 98:260–266

    Google Scholar 

  • Del Sarto MCL, Oliveira EE, Guedes RNC, Campos LAO (2014) Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera. Apidologie 45:626–636

    Google Scholar 

  • Dively GP, Kamel A (2012) Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J Agric Food Chem 60:4449–4456

  • Dorneles AL, de Souza Rosa A, Blochtein B (2017) Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi. Apidologie 48:612–620

  • El Hassani AK, Dacher M, Gary V, Lambin M, Gauthier M, Armengaud C (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Con Tox 54:653–661

    Google Scholar 

  • Felton JC, Oomen PA, Stevenson JH (1986) Toxicity and hazard of pesticides to honeybees: harmonization of the test methods. Bee World 67:114–124

    Google Scholar 

  • Free JB (1993) Insect pollination of crops. Academic Press, London

    Google Scholar 

  • Gauthier M (2010) State of the art on insect acetylcholine receptor function in learning and memory. In: Thany SH (ed) Insect nicotinic acetylcholine receptors. Advances in experimental medicine and biology, vol 683. Springer, New York, pp 97–115

    Google Scholar 

  • Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di Bernardo A, Greatti M, Giorio C, Tapparo A (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815

    CAS  Google Scholar 

  • Gradish AE, Scott-Dupree CD, Cutler GC (2012) Susceptibility of Megachile rotundata to insecticides used in wild blueberry production in Atlantic Canada. J Pest Sci 85:133–140

    Google Scholar 

  • Hardstone MC, Scott JG (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag. Sci. 66:1171–1180

    CAS  Google Scholar 

  • Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23:371–378

    CAS  Google Scholar 

  • Jacob CRO, Malaquias JB, Zanardi OZ, Silva CAS, Jacob JFO, Yamamoto PT (2019) Oral acute toxicity and impact of neonicotinoids on Apis mellifera L. and Scaptotrigona postica Latreille (Hymenoptera: Apidae). Ecotoxicology 28:744–753

  • Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    CAS  Google Scholar 

  • Jiménez DR, Cure JR (2016) Efecto letal agudo de los insecticidas em formulación comercial Imidacloprid, Spinosad y Thiocyclam hidrogenoxalato en obreras Bombus atratus (Hymenoptera: Apidae). Rev Biol Trop 64:1737–1745

    Google Scholar 

  • Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity-USA. Apidologie 41:312–331

    CAS  Google Scholar 

  • Kagabu S (1997) Chloronicotinyl insecticides - discovery, application and future perspective. Rev Toxicol 1:75–129

    CAS  Google Scholar 

  • Klein AM, Vaissiéri BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Google Scholar 

  • Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7:e29268

    CAS  Google Scholar 

  • Lambin M, Armengaud C, Raymond S, Gauthier M (2001) Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 48:129–134

    CAS  Google Scholar 

  • Laurino D, Porporato M, Patetta A, Manino A (2011) Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. Bull Insectol 64:107–113

    Google Scholar 

  • Malagodi-Braga KS, Kleinert AMP (2007) Como o comportamento das abelhas na flor do morangueiro (Fragaria ananassa Duchesne) influencia a formação dos frutos? Bioscience 23:76–81

    Google Scholar 

  • Malone LA, Scott-Dupree CD, Todd JH, Ramankutty P (2007) No sub-lethal toxicity to bumblebees, Bombus terrestris, exposed to Bt-corn pollen, captan and novaluron. New Zeal J Crop Hort 35:435–439

    CAS  Google Scholar 

  • Medrzycki P, Giffard H, Aupinel P, Belzunces LP, Chauzat MP, Claben C, Colin ME, Dupont T, Girolami V, Johnson R, Le Conte Y, Luckmann J, Marzaro M, Pistorius J, Porrini C, Schur A, Sgolastra F, Delso NS, Van der Steen JJM, Wallner C, Alaux C, Biron DG, Blot N, Bogo G, Brunet JL, Delbac F, Diogon M, El Alaouil H, Provost B, Tosi S, Vidau C (2013) Standard methods for toxicology research in Apis mellifera. J Apic Res 52:1–60

    Google Scholar 

  • Minussi LC, Alves-dos-Santos I (2007) Abelhas nativas versus Apis mellifera Linnaeus, espécie exótica (Hymenoptera: Apidae). Bioscience 23:58–62

    Google Scholar 

  • Mommaerts V, Sterk G, Smagghe G (2006) Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris. Pest Manag Sci 62:752–758

    CAS  Google Scholar 

  • Morandin LA, Winston ML, Franklin MT, Abbott VA (2005) Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Manag Sci 61:619–626

    CAS  Google Scholar 

  • Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5:e9754

    Google Scholar 

  • Nunes-Silva P, Hrncir M, Da Silva CI, Roldão YS, Imperatriz-Fonseca VL (2013) Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie 44:537–546

    Google Scholar 

  • Oliveira EE, de Souza Aguiar RW, de Almeida Sarmento R, de Souza Tuelher E, Guedes RNC (2002) Seletividade de inseticidas a Theocolax elegans parasitoide de Sitophilus zeamais. Bioscience 18:11–16

  • Padilha AC, Piovesan B, Morais MC, Pazini JB, Zotti MJ, Grützmacher AD (2020) Toxicity of insecticides on Neotropical stingless bees Plebeia emerina (Friese) and Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini). Ecotoxicology 29:119–128

    CAS  Google Scholar 

  • Pitts-Singer TL, Barbour JD (2016) Effects of residual novaluron on reproduction in alfalfa leafcutting bees, Megachile rotundata F. (Megachilidae). Pest Manag Sci 73:153–159

    Google Scholar 

  • Prado-Silveira A, Nunes LA, Dos Santos JM, Affonso PRAM, Waldschmidt AM (2018) Morphogenetic alterations in Melipona quadrifasciata anthidioides (Hymenoptera: Apidae) associated with pesticides. Arch Environ Contam Toxicol 74:627–632

    Google Scholar 

  • Ritz C, Streibig JC (2005) Bioassay Analysis using R. J Stat Softw 12:1–22

    Google Scholar 

  • Ruiz L, Flores S, Cancino J, Arredondo J, Valle J, Díazfleischer F, Williams T (2008) Lethal and sublethal effects of spinosad-based GF-120 bait on the tephritid parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biol Control 44:296–304

    CAS  Google Scholar 

  • Sánchez-Bayo F (2011) Insecticides mode of action in relation their toxicity to non-target organisms. J Environ Anal Toxicol 4:1–9

    Google Scholar 

  • Scott-Dupree CD, Conroy L, Harris CR (2009) Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J Econ Entomol 102:177–182

    CAS  Google Scholar 

  • Shi TF, Wang WF, Liu F, Qi L, Yu LS (2017) Sublethal effects of the neonicotinoid insecticide thiamethoxam on the transcriptome of the honey bees (Hymenoptera: Apidae). J Econ Entomol 20:1–7

    Google Scholar 

  • Slaa EJ, Chaves LAS, Malagodi-Braga KS, Hofsted FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315

    Google Scholar 

  • Soares HM, Jacob CRO, Carvalho SM, Nocelli RCF, Malaspina O (2015) Toxicity of imidacloprid to the stingless bee Scaptotrigona postica Latreille, 1807 (Hymenoptera: Apidae). Bull Environ Contam Toxicol 94:675–680

    CAS  Google Scholar 

  • Stein K, Coulibaly D, Stenchly K, Goetze D, Porembski S, Lindner A, Konaté S, Linsenmair EK (2017) Bee pollination increases yield quantity and quality of cash crops in Burkina Faso, West Africa. Sci Rep 7:1–10

    CAS  Google Scholar 

  • Stock D, Holloway PJ (1993) Possible mechanisms for surfactant-induced foliar uptake of agrochemicals. Pestic Sci 38:165–177

    CAS  Google Scholar 

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

    Google Scholar 

  • Tan J, Galligan JJ, Hollingworth RM (2007) Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicology 28:829–842

    CAS  Google Scholar 

  • Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015) Spinosad in the native stingless bee Melipona quadrifasciata: regrettable non-target toxicity of a bioinsecticide. Chemosphere 124:103–109

    Google Scholar 

  • Tosi S, Burgio G, Nieh JC (2017) A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Sci Rep 7:1–8

    Google Scholar 

  • Valdovinos-Núñez GF, Quezada-Euán JJG, Ancona-Xiu P, Moo-Valle H, Carmona A, Sánchez ER (2009) Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). J Econ Entomol 102:1737–1742

    Google Scholar 

  • Williams T, Valle J, Viñuela E (2003) Is the naturally-derived insecticide Spinosad compatible with insect natural enemies? Biocontrol Sci Technol 13:459–475

    Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard university press, London

    Google Scholar 

  • Witter S, Radin B, Lisboa BB, Teixeira JSG, Blochtein B, Imperatriz-Fonseca VL (2012) Desempenho de cultivares de morango submetidas a diferentes tipos de polinização em cultivo protegido. Pesqui Agropecu Bras 47:58–65

    Google Scholar 

  • Witter S, Nunes-Silva P, Blochtein B, Lisboa BB, Imperatriz-Fonseca VL (2014) As abelhas e a agricultura. EDIPUCRS, Porto Alegre

    Google Scholar 

  • Yankit P, Rana K, Sharma HK, Thakur M, Thakur RK (2018) Effect of bumble bee pollination on quality and yield of tomate (Solanum lycopersicum Mill.) grown under protected conditions. Int J Curr Microbiol App Sci 7:257–263

    Google Scholar 

  • Yu SJ (2008) The toxicology and biochemistry of insecticides. CRC Press, Boca Raton

    Google Scholar 

  • Zebrowska J (1998) Influence of pollination modes on yield components in strawberry (Fragaria x ananassa Duch.). Plant Breed 117:225–260

    Google Scholar 

Download references

Funding

To Coordination of Improvement of Higher Education Personnel (CAPES, Finance Code 001) for granting scholarships.

Author information

Authors and Affiliations

  1. Department of Crop Protection, Federal University of Pelotas, 354, Capão do Leão, 96010-900, Rio Grande do Sul, Brazil

    Bruna Piovesan, Aline Costa Padilha, Maíra Chagas Morais, Anderson Dionei Grützmacher & Moisés João Zotti

  2. Laboratory of Entomology, Brazilian Agricultural Research Corporation, 515, Bento Gonçalves, 95701-008, Rio Grande do Sul, Brazil

    Marcos Botton

Authors
  1. Bruna Piovesan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aline Costa Padilha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maíra Chagas Morais
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcos Botton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anderson Dionei Grützmacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Moisés João Zotti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruna Piovesan.

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

Piovesan, B., Padilha, A.C., Morais, M.C. et al. Effects of insecticides used in strawberries on stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi (Hymenoptera: Apidae). Environ Sci Pollut Res 27, 42472–42480 (2020). https://doi.org/10.1007/s11356-020-10191-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10191-7

Keywords

Search

Navigation