Abstract
In the last few years, with the increase in agricultural productivity, there has also been an increase in the use of insecticides to combat insects considered pests. However, these chemical compounds end up affecting nontarget insects that also interact with the crops. Studies have shown that social bees are among the insects that are suffering most from the effects of these compounds, resulting in negative ecological and economic impacts, considering that these insects provide pollination services in ecosystems. At the same time, social wasps also interact with plants, including cultivated ones, and perform ecological services similar to those of social bees, so it can be hypothesized that insecticides are also affecting social wasp colonies. Therefore, the purpose of this study was to evaluate contamination and sublethal effects of neonicotinoids on the mobility of the social wasp Protopolybia exigua (Saussure). In the first step, oral exposure experiments were performed to determine lethal and sublethal concentrations. In a second step, the wasps were exposed to sublethal concentrations, in order to evaluate the effects on their mobility. The results demonstrated that this species is more susceptible to exposure to neonicotinoids, compared to several bee species that have so far been studied, but lower than others. Exposure to sublethal concentrations can significantly reduce wasp mobility, which can have short-term consequences both for worker wasps and for the maintenance of their colonies.
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Data Availability
The datasets generated during and analysed during the current study are available from the corresponding author on reasonable request.
References
Amaro P, Utl ISA (2008) Já Há Muito Tempo que os Pesticidas Matam as Abelhas. O Apic 1965:29–40
Auteri D, Arena M, Barmaz S, Ippolito A, Linguadoca A, Molnar T, Sharp R, Szentes C, Vagenende B, Verani A (2017) Neonicotinoids and bees: the case of the European regulatory risk assessment. Sci Total Environ 579:966–971. https://doi.org/10.1016/j.scitotenv.2016.10.158
Baines D, Wilton E, Pawluk A, De Gorter M, Chomistek N (2017) Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees. Sci Rep. https://doi.org/10.1038/s41598-017-10489-6
Barros M (1998) Sistemas reprodutivos e polinização em espécies simpátricas de Erythroxylum P. Br. (Erythroxylaceae) do Brasil. Braz J Bot 21:159–166
Batista NR, de Oliveira VES, Crispim PD, Nocelli RCF, Antonialli-Junior WF (2022) Is the social wasp Polybia paulista a silent victim of neonicotinoid contamination? Environ Pollut 308:119682. https://doi.org/10.1016/j.envpol.2022.119682
Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectol 56:63–67
Bovi TS, Zaluski R, Orsi RO (2018) Toxicity and motor changes in Africanized honey bees (Apis mellifera L.) exposed to fipronil and imidacloprid. An Acad Bras Cienc 90:239–245
Bowen-Walker PL, Gunn A (2001) The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomol Exp Appl 101:207–217. https://doi.org/10.1046/j.1570-7458.2001.00905.x
Brock RE, Cini A, Sumner S (2021) Ecosystem services provided by aculeate wasps. Biol Rev 96:1645–1675. https://doi.org/10.1111/brv.12719
Camp AA, Lehmann DM (2021) Impacts of neonicotinoids on the bumble bees Bombus terrestris and Bombus impatiens examined through the lens of an adverse outcome pathway framework. Environ Toxicol Chem 40:309–322. https://doi.org/10.1002/etc.4939
Carpenter JM, Marques OM (2001) Contribuição Ao Estudo Dos Vespídeos Do Brasil. Cruz das Almas Bahia
Catae AF, Roat TC, De Oliveira RA, Ferreira Nocelli RC, Malaspina O (2014) Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of Africanized Apis mellifera (Hymenoptera: Apidae). Microsc Res Tech 77:274–281. https://doi.org/10.1002/jemt.22339
Chahbar N, Chahbar M, Doumandji S (2014) Evaluation of acute toxicity of thiamethoxam in algerian honeybee Apis mellifera intermissa and Apis mellifera sahariensis. Int J Zool 4:29–40
Clemente MA, Lange D, Del-Claro K, Prezoto F, Campos NR, Barbosa BC (2012) Flower-visiting social wasps and plants interaction: network pattern and environmental complexity. Psyche A J Entomol 2012:1–10. https://doi.org/10.1155/2012/478431
CONAB (2015) Acompanhamento da safra brasileira: grãos: safra 2014/2015: décimo segundo levantamento. https://www.conab.gov.br/info-agro/safras/graos/boletim-da-safra-de-graos/item/download/1293_ecec187e755497ccb7ac9bc816d5e319. Accessed 2 April 2022
Dorigo A, Rosa-Fontana A, Camargo I, Nocelli R, Malaspina O (2018) Biological data of stingless bees with potential application in pesticide risk assessments. Sociobiology 65:777. https://doi.org/10.13102/sociobiology.v65i4.2878
de Oliveira Ferreira MF, de Fraga R, de Barros EC , Augusto SC (2022) Effects of abamectin and acetamiprid pesticides on the survival and behavior of Scaptotrigona aff. xanthotricha (Apidae, Meliponini). J Apic Res. https://doi.org/10.1080/00218839.2020.1835262
de Oliveira Jacob CR, Zanardi OZ, Malaquias JB, Souza Silva CA, Yamamoto PT (2019) The impact of four widely used neonicotinoid insecticides on Tetragonisca angustula (Latreille) (Hymenoptera: Apidae). Chemosphere 224:65–70. https://doi.org/10.1016/j.chemosphere.2019.02.105
Dorneles AL, de Souza RA, 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
de Castro Faria ÁB (2009) Revisão sobre alguns grupos de inseticidas utilizados no manejo integrado de pragas florestais A review of some insecticide groups used in forest pest integrated management. Ambiência 5:345–358
Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419. https://doi.org/10.1016/j.ecoenv.2003.08.001
Finney DJ (1947) Probit analysis, a statistical treatment of the sigmoid response curve. Cambridge University Press, London
Guez D, Belzunces LP, Maleszka R (2003) Effects of imidacloprid metabolites on habituation in honeybees suggest the existence of two subtypes of nicotinic receptors differentially expressed during adult development. Pharmacol Biochem Behav. https://doi.org/10.1016/S0091-3057(03)00070-4
Jeanne RL (1980) Evolution of social behavior in the Vespidae. Annu Rev Entomol 25:371–396
Jeschke P, Nauen R (2008) Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098. https://doi.org/10.1002/ps.1631
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. https://doi.org/10.1002/arch.1065
Laurino D, Manino A, Patetta A, Porporato M (2013) Toxicity of neonicotinoid insecticides on different honey bee genotypes. Bull Insectol 66:119–126
Lima MC, Rocha SA (2012) Efeitos dos agrotóxicos sobre as abelhas silvestres no Brasil: proposta metodológica de acompanhamento. Ibama, Brasília
Lourenço CT, Carvalho SM, Malaspina O, Nocelli RCF (2012) Oral toxicity of fipronil insecticide against the stingless bee Melipona scutellaris (Latreille, 1811). Bull Environ Contam Toxicol 89:921–924. https://doi.org/10.1007/s00128-012-0773-x
Ludicke JC, Nieh JC (2020) Thiamethoxam impairs honey bee visual learning, alters decision times, and increases abnormal behaviors. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2020.110367
Maienfisch P, Angst M, Brandl F, Fischer W, Hofer D, Kayser H, Kobel W, Rindlisbacher A, Senn R, Steinemann A, Widmer H (2001) Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest Manag Sci 57:906–913. https://doi.org/10.1002/ps.365
Μarques-Souza AC (1996) Fontes de pólen exploradas por Melipona compressipes manaosensis (APIDAE: MELIPONINAE), abelha da amazônia central. Acta Amaz 26:77–86. https://doi.org/10.1590/1809-43921996261086
Miotelo L, Mendes dos Reis AL, Rosa-Fontana A, da Silva K, Pachú J, Malaquias JB, Malaspina O, Roat TC (2022) A food-ingested sublethal concentration of thiamethoxam has harmful effects on the stingless bee Melipona scutellaris. Chemosphere. https://doi.org/10.1016/j.chemosphere.2021.132461
Moral RA, Hinde J, Demétrio CGB (2017) Half-normal plots and overdispersed models in R : the hnp Package. J Stat Softw 81. https://doi.org/10.18637/jss.v081.i10
Nauen R, Ebbinghaus-Kintscher U, Elbert A, Jeschke P, Tietjen K (2001) Acetylcholine receptors as sites for develo** neonicotinoid insecticides. In: Ishaaya I (ed) Biochemical Sites of Insecticide Action and Resistance. Springer, Berlin, Heidelberg, pp 77–105
Navarro Z (2001) Desenvolvimento rural no Brasil: os limites do passado e os caminhos do futuro. Estud Avançados 15:83–100. https://doi.org/10.1590/S0103-40142001000300009
OECD (1998) Test No. 213: honeybees, acute oral toxicity test. OECD Guidel Test Chem pp. 1–8. https://doi.org/10.1787/9789264070165-en
Prezoto M, Detoni M, Barbosa, (2019) Pest control potential of social wasps in small farms and urban gardens. Insects 10:192. https://doi.org/10.3390/insects10070192
Quiroga Murcia DE, Zotti MJ, Zenner de polania I, Pech-Pech EE (2017) Toxicity evaluation of two insecticides on Tetragonisca angustula and Scaptotrigona xanthotricha (Hymenoptera: Apidae). Agron Colomb 35:340–349. https://doi.org/10.15446/agron.colomb.v35n3.65447
R Core Team (2019) R: a language and environment for statistical computing. R Foundation Statistical Computing
Ratnieks FLW, Carreck NL (2010) Clarity on honey bee collapse? Science (80-) 327:152–153. https://doi.org/10.1126/science.1185563
Richter MR (2000) Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu Rev Entomol 45:121–150. https://doi.org/10.1146/annurev.ento.45.1.121
Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7:e30023. https://doi.org/10.1371/journal.pone.0030023
Silva BS, Nocelli RCF, Soares MS, Malaspina O (2016) Efeitos do imidacloprido sobre o comportamento das abelhas Scaptotrigona postica Latreille, 1807 ( Hymenoptera, Apidae ). Rev Ciênc Tecnol Ambient 3:21–28
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. https://doi.org/10.1007/s00128-015-1488-6
Suhs RB, Somavilla A, Köhler A, Putzke J (2009) Vespídeos (Hymenoptera, Vespidae) vetores de pólen de Schinus terebinthifolius Raddi (Anacardiaceae), Santa Cruz do Sul, RS, Brasil. Rev Bras Biociências 7:138–143
Tadei R, Domingues CEC, Malaquias JB, Camilo EV, Malaspina O, Silva-Zacarin ECM (2019) Late effect of larval co-exposure to the insecticide clothianidin and fungicide pyraclostrobin in Africanized Apis mellifera. Sci Rep 9:3277. https://doi.org/10.1038/s41598-019-39383-z
Tadei R, Menezes-Oliveira VB, Silva-Zacarin ECM (2020) Silent effect of the fungicide pyraclostrobin on the larval exposure of the non-target organism Africanized Apis mellifera and its interaction with the pathogen Nosema ceranae in adulthood. Environ Pollut 267:115622. https://doi.org/10.1016/j.envpol.2020.115622
Teixeira I, Botton M, Loeck AE (2002) Avaliação de Inseticidas Visando ao Controle de Eurhizococcus brasiliensis (Hempel) (Hemiptera: Margarodidae) em Novos Plantios de Videira. Neotrop Entomol 31:457–461. https://doi.org/10.1590/S1519-566X2002000300017
Teixeira GVM, De Souza AR, Barbosa WF, Bernardes RC, Lima MAP (2022) Chronic exposure to a common biopesticide is detrimental to individuals and colonies of the paper wasp Polistes versicolor. Sci Total Environ 810:152108. https://doi.org/10.1016/j.scitotenv.2021.152108
Thompson H, Overmyer J, Feken M, Ruddle N, Vaughan S, Scorgie E, Bocksch S, Hill M (2019) Thiamethoxam: long-term effects following honey bee colony-level exposure and implications for risk assessment. Sci Total Environ 654:60–71. https://doi.org/10.1016/j.scitotenv.2018.11.003
Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 48:339–364. https://doi.org/10.1146/annurev.ento.48.091801.112731
Tosi S, Burgio G, Nieh JC (2017) A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Sci Rep 7:1201. https://doi.org/10.1038/s41598-017-01361-8
Tsvetkov N, Samson-Robert O, Sood K, Patel HS, Malena DA, Gajiwala PH, Maciukiewicz P, Fournier V, Zayed A (2017) Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science (80-) 356:1395–1397. https://doi.org/10.1126/science.aam7470
Wagner DL, Grames EM, Forister ML, Berenbaum MR, Stopak D (2021) Insect decline in the Anthropocene: death by a thousand cuts. Proc Natl Acad Sci 118:1–10. https://doi.org/10.1073/pnas.2023989118
Wenzel JW (1980) A generic key to the nests of hornets, yellowjackets, ans paper wasps worldwide (Vespidae: Vespinae, Polistinae). Am Museum Novit 3224:1–39
Wilson EO (1971) The insect societies. Cambridge, Massachusetts
Funding
The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) – funding code 001. In addition to Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (concession numbers: 308182/2019–7 WFAJ and 400540/2018–5 RCFN), and to São Paulo Research Foundation (FAPESP) for supporting this study with grants 2017/21097–3 (RCFN).
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Paula Danyelle Crispim: conceptualization, methodology, investigation, data curation, writing — original draft, visualization. Vinicius Edson Soares de Oliveira: methodology, investigation. Nathan Rodrigues Batista: methodology, investigation, formal analysis, data curation, writing — review and editing. Roberta Cornélio Ferreira Nocelli: conceptualization, validation, writing — review and editing, visualization, supervision. William Fernando Antonialli-Junior: conceptualization, validation, resources, writing — review and editing, visualization, supervision, project administration, funding acquisition.
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Crispim, P.D., de Oliveira, V.E.S., Batista, N.R. et al. Lethal and Sublethal Dose of Thiamethoxam and Its Effects on the Behavior of a Non-target Social Wasp. Neotrop Entomol 52, 422–430 (2023). https://doi.org/10.1007/s13744-023-01028-2
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DOI: https://doi.org/10.1007/s13744-023-01028-2