Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-20T22:52:14.609Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in Synapsin Levels in the Millipede Gymnostreptus olivaceus Schubart, 1944 Exposed to Different Concentrations of Deltamethrin

Published online by Cambridge University Press:  08 January 2016

Annelise Francisco ,
Pablo H. Nunes ,
Roberta C. F. Nocelli  and
Carmem S. Fontanetti
Annelise Francisco
Affiliation:
Departamento de Biologia, Instituto de Biociências de Rio Claro, Universidade Estadual Paulista (UNESP), Bela Vista, 13.500-900, Rio Claro, São Paulo, Brazil
Pablo H. Nunes
Affiliation:
Centro Interdisciplinar de Ciências da Vida e da Natureza (CICV), Instituto Latino-Americano de Ciências da vida e da Natureza (ILACVN), Universidade Federal da Integração Latino-Americana (UNILA), Avenida Silvio Américo Sasdelli, 1842, 85.866-000, Foz do Iguaçu, Paraná, Brazil
Roberta C. F. Nocelli
Affiliation:
Departamento de Ciências da Natureza, Matemática e Educação, Centro de Ciências Agrárias, Universidade Federal de São Carlos (UFSCar), Via Anhanguera, Km 174, 13.600-970, Araras, São Paulo, Brazil
Carmem S. Fontanetti*
Affiliation:
Departamento de Biologia, Instituto de Biociências de Rio Claro, Universidade Estadual Paulista (UNESP), Bela Vista, 13.500-900, Rio Claro, São Paulo, Brazil
*
*Corresponding author.fontanet@rc.unesp.br
Get access

Abstract

Millipedes are ecologically important soil organisms and may also be an economically threatening species in rural and urban areas when population outbreaks occur. In order to control infestations commercial formulations of deltamethrin have been commonly applied, even though there are few studies about the effects of such insecticide on millipedes. This paper describes the effects of this insecticide on millipedes showing neurotoxic effects assessed by synapsin labeling and confocal microscopy. Deltamethrin concentrations related to the DL50 of the active ingredient and a field concentration were applied topically in the diplopod Gymnostreptus olivaceus to evaluate the behavior, mortality rate, and synapsin levels in the brain 12, 24, and 48h after contact with deltamethin. The insecticide caused mortality at the higher concentrations employed, in which no change was observed in neurotransmission in the survivors. In contrast, at field concentrations, deltamethrin did not cause any deaths, but triggered significant changes in synapsin levels. The results obtained form the synapsin labeling provide several interpretations suggesting that the isolated application of this tool must be associated with additional tools in order to evaluate biologically induced effects of deltamethrin in an accurate way. In addition, the feasibility of chemical control of millipedes with deltamethrin is questioned.

Keywords

arthropodconfocal microscopydiplopodolfactory glomerulipyrethroid
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 1 , February 2016 , pp. 48 - 54
Copyright
© Microscopy Society of America 2016 

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

Arab, A., Zacarin, G.G., Fontanetti, C.S., Camargo-Mathias, M.I., Santos, M.G. & Cabrera, A.C. (2003). Composition of the defensive secretion of the Neotropical millipede Rhinocricus padbergi Verhoeff 1938 (Diplopoda: Spirobolida: Rhinocricidae). Entomotropica 18, 79–82.Google Scholar
Badiou, A. & Belzunces, L.P. (2008). Is acetylcholinesterase a pertinent biomarker to detect exposure of pyrethroids? A study case with deltamethrin. Chem Biol Interact 175, 406–409.CrossRefGoogle ScholarPubMed
Badiou, A., Meled, M. & Belzunces, L.P. (2008). Honeybee Apis mellifera acetylcholinesterase—A biomarker to detect deltamethrin exposure. Ecotoxicol Environ Saf 69, 246–253.CrossRefGoogle ScholarPubMed
Benfenati, F. (2011). Synapsins—Molecular function, development and disease. Semin Cell Dev Biol 22, 377.CrossRefGoogle ScholarPubMed
Boccardo, L., Fernandes, M.N. & Penteado, C.H.S. (2001). Toxicity of deltamethrin pyrethroid on neotropical millipedes, Gymnostreptus olivaceus and Plusioporus setiger. J Adv Zool 22, 1–4.Google Scholar
Boccardo, L., Jucá-Chagas, R. & Penteado, C.H.S. (2002). Migration and population outbreaks of millipedes in the coffee plantations, region of Alto Paranaíba, MG, Brazil. Holos Environ 2, 220–223.CrossRefGoogle Scholar
Bressan, J.M.A., Benz, M., Oettler, J., Heinze, J., Hartenstein, V. & Sprecher, S. (2014). A map of brain neuropils and fiber systems in the ant Cardiocondyla obscurior. Front Neuroanat 8, article no. 166, 12pp.Google ScholarPubMed
Cesca, F., Baldelli, P., Valtorta, F. & Benfenati, F. (2010). The synapsins: Key actors of synapse function and plasticity. Prog Neurobiol 91, 313–348.CrossRefGoogle ScholarPubMed
Chen, D., Huang, X., Liu, L. & Shi, N. (2007). Deltamethrin induces mitochondrial membrane permeability and altered expression of cytochrome C in rat brain. J Appl Toxicol 27, 368–372.CrossRefGoogle ScholarPubMed
Chi, P., Greengard, P. & Ryan, T.A. (2003). Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38, 69–78.CrossRefGoogle ScholarPubMed
Clark, J.M. & Matsumura, F. (1982). Two different types of inhibitory effects of pyrethroids on nerve Ca- and Ca+ Mg- ATPase activity in the squid, Loligo pealei. Pestic Biochem Physiol 18, 180–190.CrossRefGoogle Scholar
Cloudslaey-Thompson, J.L. (1949). Significance of migration in myriapods. Naturalist 2, 947–962.Google Scholar
Decourtye, A., Devillers, J., Cluzeau, S., Charreton, M. & Pham-Delègue, M. (2004). Effects of imadacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57, 410–419.CrossRefGoogle ScholarPubMed
Diegelmann, S., Klagges, B., Michels, B., Schleyer, M. & Gerber, B. (2013). Maggot learning and synapsin function. J Exp Biol 216, 939–951.CrossRefGoogle ScholarPubMed
Ebregt, E., Struik, P.C., Abidin, P.E. & Odongo, B. (2004 a). Farmers’ information on sweet potato production and millipede infestation in north-eastern Uganda I. Associations between spatial and temporal crop diversity and the level of pest infestation. W J Life Sci 52, 47–68.Google Scholar
Ebregt, E., Struik, P.C., Abidin, P.E. & Odongo, B. (2004 b). Farmers’ information on sweet potato production and millipede infestation in north-eastern Uganda II. Pest incidence and indigenous control strategies. W J Life Sci 54, 70–84.Google Scholar
Eriksson, P. & Fredriksson, A. (1991). Neurotoxic effects of two different pyrethroids, bioallethrin and deltamethrin, on immature and adult mice: Changes in behavioral and muscarinic receptor variables. Toxicol Appl Pharmacol 108, 78–85.CrossRefGoogle ScholarPubMed
Fontanetti, C.S. (1989). Moulting behaviour in Chelodesmid species (Diplopoda, Polydesmida). Rev Bras Biol 49, 1053–1055.Google Scholar
Fontanetti, C.S., Calligaris, I.B. & Souza, T.S. (2010). A millipede infestation of an urban area of the city of Campinas, Brazil and premilinary toxicity studies of insecticide Bendiocarb® to the Urostreptus atrobrunneus Pierozzi & Fonatnetti, 2006. Arq Inst Biol São Paulo 77, 165–166.CrossRefGoogle Scholar
Francisco, A., Nocelli, R.C.F. & Fontanetti, C.S. (2015). The nervous system of the neotropical millipede Gymnostreptus olivaceus Schubart, 1944 (Spirostreptida, Spirostreptidae) shows an additional cell layer. Anim Biol 65, 133–150.CrossRefGoogle Scholar
Girardin, B.W. & Stevesons, S. (2002). Millipedes—Health consequences. J Emerg Nurs 28, 107–110.CrossRefGoogle ScholarPubMed
Golovatch, S.I. & Kime, D. (2009). Millipede (Diplopoda) distribuitions: A review. Soil Organ 81, 565–597.Google Scholar
Groh, C., Kelber, C., Grübel, K. & Rössler, W. (2014). Density of mushroom body synaptic complexes limits intraspecies brain miniaturization in highly polymorphic leaf-cutting ant workers. Proc R Soc B 281, 1–9.CrossRefGoogle ScholarPubMed
Groh, C., Tautz, J. & Rössler, W. (2004). Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proc Natl Acad Sci U S A 101, 4268–4273.CrossRefGoogle ScholarPubMed
Hifiker, S., Pieribone, V.A., Czernik, A.J., Kao, H., Augustine, G.J. & Greengard, P. (1999). Synapsin as regulators of neurotransmitter release. Philos Trans R Soc B 354, 269–279.CrossRefGoogle Scholar
Hopkin, S.P. & Read, H. J. (1992). The Biology of Millipedes. New York, NY, USA: Oxford University Press.CrossRefGoogle Scholar
Hoyer, S. C., Liebig, J. & Rössler, W. (2005). Biogenic amines in the ponerine ant Harpegnathos saltator serotonin and dopamine immunoreactivity in the brain. Arthropod Struct Dev 34, 429–440.CrossRefGoogle Scholar
Humeau, Y., Candiani, S., Ghirardi, M., Poulain, B. & Montarolo, P. (2011). Functional roles of synapsins: Lessons from invertebrates. Semin Cell Dev Biol 22, 425–433.CrossRefGoogle ScholarPubMed
Huttner, W.B., Schiebler, W., Greengard, P. & DE Camilli, P. (1983). Synapsin I (protein I), a nerve terminal-especific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96, 1374–1388.CrossRefGoogle Scholar
Larini, L. (1999). Inseticidas Organossintéticos. In Toxicologia dos praguicidas, Larini, L. (Ed.), pp. 19–91. São Paulo: Editora Manole Ltda.Google Scholar
Leitinger, G., Pabst, M.A., Rind, F.C. & Simmons, P.J. (2004). Differential expression of synapsin in visual neurons of the locust Schistocerca gregaria. J Comp Neurol 480, 89–100.CrossRefGoogle ScholarPubMed
Lordello, L.G.E. (1954). Observações sobre alguns diplópodos de interesse agrícola. Anais da E S A “Luiz de Queiroz” 11, 69–79.Google Scholar
Marôco, J. (2014). Análise Estatística com o SPSS Statistics. Pêro Pinheiro: Gráfica Manuel Barbosa & Filhos.Google Scholar
McCavera, S.J. & Soderlund, D.M. (2012). Differential state-dependent modification of inactivation-deficient Na v1.6 sodium channels by the pyrethroid insecticides S-bioallethrin, tefluthrin and deltamethrin. Neurotoxicology 33, 384–390.CrossRefGoogle Scholar
Niijima, K. & Shinohara, K. (1988). Outbreaks of the Parafontaria laminata group (Diplopoda: Xystodesmidae). Jpn J Ecol 38, 257–268.Google Scholar
Orchard, I. (1980). The effects of pyrethroids on the electrical activity of neurosecretory cells from the brain on Rhodnius prolixus. Pestic Biochem Physiol 13, 220–226.CrossRefGoogle Scholar
Ott, S.R. (2008). Confocal microscopy in large insect brains: Zinc-formaldehyde fixation improves synapsin immunostaining and preservation of morphology in whole-mounts. J Neurosci Methods 172, 220–230.CrossRefGoogle ScholarPubMed
Petersen, H. & Luxton, M. (1982). A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 291–357.CrossRefGoogle Scholar
Romell, L.G. (1935). An example of myriapods as mull formers. Ecology 16, 67–71.CrossRefGoogle Scholar
Ruppert, E.E., Fox, R.S. & Barnes, R.D. (2005). Myriapoda. In Zoologia dos invertebrados—Uma abordagem funcional-evolutiva, Ruppert, E.E., Fox, R.S. & Barnes, R.D. (Eds.), pp. 819–842. São Paulo: Editora Roca Ltda.Google Scholar
Scharf, M.E. (2003). Neurological effects of insecticides. In Encyclopedia of Pest Management, Pimentel, D. (Ed.), pp. 395–399. Boca Raton, FL: CRC Press.Google Scholar
Schubart, O. (1942). Os Myriapodes e suas relações com a agricultura. Pap Avulsos Dep Zool Secr Agric Ind Comer (São Paulo) 2, 205–234.Google Scholar
Soderlund, D.M. & Bloomquist, J.R. (1989). Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34, 77–96.CrossRefGoogle ScholarPubMed
Soderlund, D.M., Clark, J.M., Sheets, L.P., Mullin, L.S., Piccirillo, V.J., Sargent, D., Stevens, J.T. & Weiner, M.L. (2002). Mechanisms of pyrethroid neurotoxicity: Implications for cumulative risk assessment. Toxicology 171, 3–59.CrossRefGoogle ScholarPubMed
Sombke, A., Harzsch, S. & Hansson, B.S. (2011). Organization of deutocerebral neuropils and olfactory behavior in the centipede Scutigera coleoptrata (Linnaeus, 1758) (Myriapoda: Chilopoda). Chem Senses 36, 43–61.CrossRefGoogle ScholarPubMed
Wightman, J.A. & Wightman, A.S. (1994). An insect and sociological survey of groundnut fields in southern Africa. Agric Ecosyst Environ 51, 311–331.CrossRefGoogle Scholar
Winder, G.H., Dewar, A.M. & Dunning, R.A. (1993). Comparisons of granular pesticides for the control of soil-inhabiting arthropod pests of sugar beet. Crop Prot 12, 148–154.CrossRefGoogle Scholar
Wu, A. & Liu, Y. (2000 a). Apoptotic cell death in rat brain following deltamethrin treatment. Neurosci Lett 279, 85–88.CrossRefGoogle ScholarPubMed
Wu, A. & Liu, Y. (2000 b). Deltamethrin induces delayed apoptosis and altered expression of p53 and bax in rat brain. Environ Toxicol Pharmacol 8, 183–189.CrossRefGoogle ScholarPubMed
Zhou, T., Zhou, W., Wang, Q., Dai, P., Liu, F., Zhang, Y. & Sun, J. (2011). Effects of pyrethroids on neuronal excitability of adult honeybees Apis mellifera. Pestic Biochem Physiol 100, 35–40.CrossRefGoogle Scholar