Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T11:42:39.910Z Has data issue: false hasContentIssue false
  • English
  • Français

Transmission Electron Microscopy as a Tool to Study the Toxicological Effects of Thiamethoxam in Workers of Atta sexdens (Myrmicinae, Attini)

Published online by Cambridge University Press:  07 December 2020

Silvana B. Poiani Open the ORCID record for Silvana B. Poiani [Opens in a new window] ,
Mayara C. Pereira  and
Odair C. Bueno
Silvana B. Poiani*
Affiliation:
Department of Biology, Sao Paulo State University (UNESP), Institute of Biosciences – Campus Rio Claro, Center of Study of Social Insects, Avenida 24A, 1515, Bela Vista, Rio Claro, SP13506-900, Brazil
Mayara C. Pereira
Affiliation:
Department of Biology, Sao Paulo State University (UNESP), Institute of Biosciences – Campus Rio Claro, Center of Study of Social Insects, Avenida 24A, 1515, Bela Vista, Rio Claro, SP13506-900, Brazil
Odair C. Bueno
Affiliation:
Department of Biology, Sao Paulo State University (UNESP), Institute of Biosciences – Campus Rio Claro, Center of Study of Social Insects, Avenida 24A, 1515, Bela Vista, Rio Claro, SP13506-900, Brazil
*
*Author for correspondence: Silvana B. Poiani, E-mail: [email protected]
Get access

Abstract

Thiamethoxam is a neonicotinoid that has been used to control insect pests. The literature reports a few behavioral studies evaluating the toxic effect of thiamethoxam in ants; however, there are scarce studies at the cellular level. The present research evaluated the effects of thiamethoxam in labial (LG) and mandibular glands (MG), fat bodies (FB), and Malpighian tubules (MT) of workers of Atta sexdens, using transmission electron microscopy. The duct and secretory cells of LG were profoundly affected, then the production of saliva can be compromised, as well as its quality and subsequent use. In MG, reservoir and canaliculi cells presented slight alterations; however, MG secretory cells presented vacuoles containing lamellar structures, increased lipid production, and a large amount of mitochondria, which may lead to organ's malfunctioning. The FB cell alterations do not seem enough to cause significant changes that lead to cell death. Prominent changes in MT, such as loss of the electron-dense concentric ring, increased smooth endoplasmic reticulum, loss of basal infolds, vacuoles containing mineralized granules, and lamellar structures associated with mitochondria, suggest that their excretory function is compromised. In conclusion, thiamethoxam acts not only in the nervous system but also contributes to systemic toxicity on the target organism.

Keywords

cell alterationsexocrine glandsneonicotinoidpesticideMalpighian tubules
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 1 , February 2021 , pp. 170 - 186
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amaral, JB & Machado-Santelli, GM (2008). Salivary system in leaf-cutting ants (Atta sexdens rubropilosa Forel, 1908) castes: A confocal study. Micron 39, 1222–1227.CrossRefGoogle ScholarPubMed
Arab, A & Caetano, FH (2002). Segmental specializations in the Malpighian tubules of the fire ant Solenopsis saevissima Forel 1904 (Myrmicinae): An electron microscopical study. Arthropod Struct Dev 30, 281–292.CrossRefGoogle Scholar
Arismendi-Morillo, G (2009). Electron microscopy morphology of the mitochondrial network in human cancer. Int J Biochem Cell Biol 41, 2062–2068.CrossRefGoogle ScholarPubMed
Ayre, GL (1963). Feeding behaviour and digestion in Camponotus herculeanus (L.) (Hymenoptera: Formicidae). Entomol Exp Appl 6, 165–170.CrossRefGoogle Scholar
Billen, J (2015). Insect exocrine glands. Arthropod Struct Dev 44, 399–400.CrossRefGoogle ScholarPubMed
Billen, J & Morgan, ED (1998). Pheromone communication in social insects: Sources and secretions. In Pheromone Communication in Social Insects, Vander-Meer, RK, Breed, MD, Espelie, KE & Winston, ML (Eds.), pp. 3–33. Boulder, Colorado: Westview Press.Google Scholar
Birch, M (1974). Aphrodisiac pheromones in insects. In Pheromones, Birch, MC (Ed.), p. 115. Amsterdam: North-Holland Publishing.Google Scholar
Bonmatin, JM, Giorio, C, Girolami, V, Goulson, D, Kreutzweiser, DP, Krupke, C, Liess, M, Long, E, Marzaro, M, Mitchell, EA, Noome, DA, Simon-Delso, N & Tapparo, A (2015). Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res Int 22, 35–67.CrossRefGoogle ScholarPubMed
Britto, JS, Forti, LC, Oliveira, MA, Zanetti, R, Wilcken, CF, Zanuncio, JC, Loeck, AE, Caldato, N, Nagamoto, NS, Lemes, PG & Camargo, RS (2016). Use of alternatives to PFOS, its salts and PFOSF for the control of leaf-cutting ants Atta and Acromyrmex. Int J Res Environ Std 3, 11–92.Google Scholar
Bromilow, RH & Chamberlain, K (1995). Principles Governing Uptake and Transport of Chemicals. Plant Contamination: Modelling and Simulation. London: Lewis Publishers.Google Scholar
Buczkowski, G, Roper, E & Chin, D (2014 a). Polyacrylamide hydrogels: An effective tool for delivering liquid baits to pest ants. J Econ Entomol 107, 748–757.CrossRefGoogle ScholarPubMed
Buczkowski, G, Roper, E, Chin, D, Mothapo, N & Wossler, T (2014 b). Hydrogel baits with low-dose thiamethoxam for sustainable Argentine ant management in commercial orchards. Entomol Exp Appl 153, 183–190.CrossRefGoogle Scholar
Bueno, OC, Morini, MSC, Pagnocca, FC, Hebling, MJAH & Silva, O (1997). Sobrevivência de operárias de Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) isoladas do formigueiro e alimentadas com dietas artificiais. An Soc Entomol Bras 26, 107–113.CrossRefGoogle Scholar
Buschinger, A & Maschwitz, U (1984). Defensive behavior and defensive mechanisms in ants. In Defensive Mechanisms in Social Insects, Hermann, HR (Ed.), pp. 95–150. New York: Praeger.Google Scholar
Bution, ML, Caetano, FH & Zara, FJ (2008). Contribution of the Malpighian tubules for the maintenance of symbiotic microorganisms in Cephalotes ants. Micron 39, 1179–1183.CrossRefGoogle ScholarPubMed
Caetano, FH & Cruz-Landim, C (1983). Ultrastructure of columnar cells from ventricle of Camponotus arboreus (Hymenoptera: Formicidae) and their functional implications. Naturalia 8, 91–100.Google Scholar
Caetano, FH, Jaffé, K & Zara, FJ (2002). Formigas: biologia e anatomia. Araras, Brazil: Editora Topásio.Google Scholar
Chapman, RF (2013). The Insects: Structure and Function. Simpson, SJ & Douglas, AE (Eds.). New York, USA: Cambridge University Press.Google Scholar
Claude, A (1970). Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. I. Elaboration of elements of the Golgi complex. J Cell Biol 47, 745–766.CrossRefGoogle ScholarPubMed
Cruz-Landim, C (1967). Estudo comparativo de algumas glândulas das abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq Zool 15, 177–290.CrossRefGoogle Scholar
Cruz-Landim, C (1990). Cephalic exocrine glands of ants: A morphological view. In Applied Myrmecology: A World Perspective, Vander Meer, RK, Jaffe, K & Cedeno, A (Eds.), pp. 102–118. New York: Westview Press.Google Scholar
Cruz-Landim, C (2002). Tipos de células secretoras presentes nas glândulas exócrinas das abelhas. In Glândulas exócrinas das abelhas, Cruz-Landim, C & Abdalla, FC (Eds.), pp. 1–20. Ribeirão Preto: FUNPEC-RP.Google Scholar
Cruz-Landim, C & Silva de Moraes, RLM (1977). Estruturas degenerativas nas glândulas hipofaríngeas de operárias de Apis mellifera (Apidae). Rev Brasil Biol 37, 681–692.Google Scholar
Daane, KM, Cooper, ML, Sime, KR, Nelson, EH, Battany, MC & Rust, MK (2008). Testing baits to control Argentine ants (Hymenoptera: Formicidae) in vineyards. J Econ Entomol 101, 699–709.CrossRefGoogle Scholar
Dean, RL, Locke, M & Collins, JV (1985). Structure of fat body. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, Kerkut, GA & Gilbert, LI (Eds.), pp. 155–210. Oxford: Pergamon Press.Google Scholar
Decio, P, Silva-Zacarin, ECM, Bueno, FC & Bueno, OC (2013). Toxicological and histophatological effects of hydramethylnon on Atta sexdens rubropilosa (Hymenoptera: Formicidae) workers. Micron 45, 22–31.CrossRefGoogle Scholar
Delage, B (1968). Recherches sur les fourmis moissoneuses du Bassin Aquitain: éthologie, physiologie de l'alimentation. Ann Sci Nat Zool 10, 197–265.Google Scholar
Della Lucia, TMC (2011). As formigas cortadeiras: da biologia ao manejo. Viçosa, Brazil: Editora da Universidade Federal de Viçosa.Google Scholar
Della Lucia, TMC, Gandra, LC & Guedes, RN (2014). Managing leaf-cutting ants: Peculiarities, trends and challenges. Pest Manag Sci 70, 14–23.CrossRefGoogle ScholarPubMed
Ensley, SM (2018). Neonicotinoids. In Veterinary Toxicology: Basic and Clinical Principles, Gupta, RC (Ed.), pp. 521–523. Amsterdam: Academic Press/Elsevier.Google Scholar
Erthal, M Jr, Silva, CP & Samuels, RI (2004). Digestive enzymes of leaf-cutting ants, Acromyrmex subterraneus (Hymenoptera: Formicidae: Attini): Distribution in the gut of adult workers and partial characterization. J Insect Physiol 50, 881–891.CrossRefGoogle ScholarPubMed
Fan, YJ, Shi, XY & Gao, X-W (2012). Research progresses on the metabolism of neonicotinoids imidacloprid and thiamethoxam. Chin J Pest Sci 14, 587–596.Google Scholar
Febvay, G & Kermarrec, A (1984). Digestion of chitin by the labial gland of Acromyrmex octospinosus Reich (Hymenoptera, Formicidae). Can J Zool 62, 229–234.CrossRefGoogle Scholar
França, SM, Breda, MO, Barbosa, DRS, Araujo, AMN & Guedes, CA (2017). The sublethal effects of insecticides in insects. In Biological Control of Pest and Vector Insects, Shields VDC (Ed.). IntechOpen. doi:10.5772/66461. Available at: https://www.intechopen.com/books/biological-control-of-pest-and-vector-insects/the-sublethal-effects-of-insecticides-in-insects.Google Scholar
Gonçalves, FC (2004). Morfologia e morfometria das glândulas mandibulares em reprodutores de Coptotermes gestroi (Isoptera, Rhinotermitidae). Dissertação (Mestrado em Biologia Celular e Molecular). Unesp. Rio Claro, SP, 64 pp.Google Scholar
Gonçalves, WG, Fialho, MDCQ, Azevedo, DO, Zanuncio, JC & Serrão, JE (2014). Ultrastructure of the excretory organs of Bombus morio (Hymenoptera: Bombini): Bee without rectal pads. Microsc Microanal 20, 285–295.CrossRefGoogle ScholarPubMed
Goulson, D (2013). An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50, 977–987.CrossRefGoogle Scholar
Gupta, RC, Miller Mukherjee, IR, Malik, JK, Doss, RB, Dettbarn, W-D & Milatovic, D (2019). Insecticides. In Biomarkers in Toxicology, Gupta, RC (Ed.), pp. 455–475. London, United Kingdom: Academic Press.CrossRefGoogle Scholar
Hölldobler, B & Wilson, OE (1990). The Ants. Berlin: Springer.CrossRefGoogle Scholar
Inoue-Yamauchi, A & Oda, H (2012). Depletion of mitochondrial fission factor DRP1 causes increased apoptosis in human colon cancer cells. Biochem Biophys Res Commun 421, 81–85.CrossRefGoogle ScholarPubMed
Leal, IR, Wirth, R & Tabarelli, M (2011). Dispersão de sementes por formigas-cortadeiras. In Formigas-cortadeiras: da biologia ao controle, Della Lucia, TMC (Ed.), pp. 236–248. Viçosa (MG), Brazil: Editora da Universidade Federal de Viçosa.Google Scholar
Maienfisch, P, Angst, A, 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.CrossRefGoogle ScholarPubMed
Marsaro Junior, AL, Lucia, TMCD, Barbosa, LCA, Maffia, LA & Morandi, MAB (2001). Inhibition of the germination of Botrytis cinerea Pers. Fr. Conidia by extracts of the mandibular glands of Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae). Neotrop Entomol 30, 403–406.CrossRefGoogle Scholar
Michener, CD (1974). The Social Behavior of the Bees: A Comparative Study. Cambridge, MA: The Belknap Press of Harvard University.Google Scholar
Moreira, DR, Sinópolis Gigliolli, AA, Falco, JRP, Julio, AHF, Volnistem, EA, Chagas, FD, 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.CrossRefGoogle Scholar
Nauen, R, Ebbinghaus-Kintscher, U, Salgado, VL & Kaussmann, M (2003). Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pest Biochem Physiol 76, 55–69.CrossRefGoogle Scholar
Nelson, EH & Daane, KM (2007). Improving liquid bait programs for Argentine ant control: Bait station density. Environ Entomol 36, 1475–1484.CrossRefGoogle ScholarPubMed
Niranjan, BG, Bhat, NK & Avadhani, NG (1982). Preferential attack of mitochondrial DNA by aflatoxin B1 during hepatocarcinogenesis. Science 215, 73–75.CrossRefGoogle ScholarPubMed
Nixon, RA (2007). Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 120, 4081–4091.CrossRefGoogle ScholarPubMed
Nocelli, R, Cintra-Socolowski, P, Roat, T, Silva-Zacarin, E & Malaspina, O (2016). Comparative physiology of malpighian tubules: Form and function. Open Access Insect Physiol 6, 13–23.Google Scholar
Ortiz, G, Vieira, AS & Bueno, OC (2017). Toxicological and morphological comparative studies of insecticides action in leaf-cutting ants. Int J Agric Innov Res 6, 516–522.Google Scholar
Pavon, LF & Camargo-Mathias, MI (2005). Ultrastructural studies of the mandibular glands of the minima, media and soldier ants of Atta sexdens rubropilosa (Forel, 1908) (Hymenoptera: Formicidae). Micron 36, 449–460.CrossRefGoogle Scholar
Poiani, SB & Cruz-Landim, C (2009). Cephalic salivary gland ultrastructure of worker and queen eusocial bees (Hymenoptera, Apidae). Anim Biol 59, 299–311.Google Scholar
Quennedey, A (1971). Les glandes exocrines dês Térmites. I. Etude histochimique et ultrastructurale de la glande sternale de Kalotermes flavicollis Fab. (Isoptera, Kalotermitidae). Z Zellforsch 121, 27–47.CrossRefGoogle Scholar
Rehman, J, Zhang, HJ, Toth, PT, Zhang, Y, Marsboom, G, Hong, Z, Salgia, R, Husain, AN, Wietholt, C & Archer, SL (2012). Inhibition of mitochondrial fission prevents cell cycle progression in lung cancer. ASEB J 26, 2175–2186.Google ScholarPubMed
Ribeiro, EM (1999). Histologia, histoquímica e ultra-estrutura da glândula intramandibular de Cephalotes (Zacryptocerus) pusillus, Andrade & Baroni, 1999 (Hymenoptera: Formicidae). Dissertação (Mestrado em Biologia Celular e Molecular). IB-UNESP.Google Scholar
Rocha, T & Caetano, FH (2004). Ultrastructure of the thoracic salivary gland of Polistes versicolor (Olivier, 1791) (Hymenoptera, Vespidae). Braz J Morphol Sci 21, 59–64.Google Scholar
Rodrigues, A, Carletti, CD, Bueno, OC & Pagnocca, FC (2008). Leaf-cutting ant faecal fluid and mandibular gland secretion effects on microfungi spore germination. Braz J Microbiol 39, 64–67.CrossRefGoogle ScholarPubMed
Roma, GC, Bueno, OC & Camargo-Mathias, MI (2009). Ultrastructural analysis of the fat body in workers of Attini ants (Hymenoptera: Formicidae). Anim Biol 59, 241–262.CrossRefGoogle Scholar
Singh, KK, Russell, J, Sigala, B, Zhang, Y, Williams, J & Keshav, KF (1999). Mitochondrial DNA determines the cellular response to cancer therapeutic agents. Oncogene 18, 6641–6646.CrossRefGoogle ScholarPubMed
Sparks, TC & Nauen, R (2015). IRAC: Mode of action classification and insecticide resistance management. Pest Biochem Physiol 121, 122–128.CrossRefGoogle ScholarPubMed
Srinivasan, S & Avadhani, NG (2012). Cytochrome c oxidase dysfunction in oxidative stress. Free Radic Biol Med 53, 1252–1263.CrossRefGoogle ScholarPubMed
Srinivasan, S, Guha, M, Kashina, A & Avadhani, NG (2017). Mitochondrial dysfunction and mitochondrial dynamics – The cancer connection. Biochim Biophys Acta 1858, 602–614.CrossRefGoogle ScholarPubMed
Wilson, EO (1971). The Insect Societies. Cambridge, MA: Belknap Press of Harvard University Press.Google Scholar