Abstract
The present study demonstrated the effects of dinotefuran (active compound of the Protetor Pet® acaricide) in germ cells and the digestive processes of semi-engorged females of R. sanguineus exposed to different concentrations of the chemical. For this purpose, 120 semi-engorged females were divided into four treatment groups with 30 individuals each: group I or control (distilled water), group II (5000 ppm), group III (6250 ppm), and group IV (8334 ppm of dinotefuran). All ticks were immersed in different concentrations of dinotefuran or in distilled water for 5 min and then were dried and stored in biological oxygen demand (BOD) incubator for 7 days. The results show the action of this compound, exhibiting morphohistologic and histochemical changes in the oocytes and the midgut cells of individuals of different groups, which were compared with those of group I (control). The alterations occurred mainly in relation to the size of the germ cells and yolk granules; presence, quantity, size, and location of vacuoles found in the cytoplasm of these germ cells; the damage occurred in the generative cells of the midgut; the size of the digestive cells; the quantity of blood elements captured, accumulated digestive wastes and digestive vacuoles found in the cytoplasm of the digestive cells of the midgut, as well as the amount and distribution of proteins, polysaccharides, lipids of all cells in both organs. So, it has demonstrated the effectiveness of dinotefuran in the reduction of fertility and digestive processes of semi-engorged females of R. sanguineus, data that points the possibility of employing this chemical to control these ectoparasites.
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References
Agbede R, Kemp D (1985) Digestion in the cattle-tick Boophilus microplus: light microscope study of the gut cells in nymphs and females. Int J Parasitol 15:147–157. doi:10.1016/0020-7519(85)90080-3
Agyei A, Runham N (1995) Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipicephalus appediculatus during digestion of the blood meal. Int J Parasitol 25:55–62. doi:10.1016/0020-7519(94)00114-4
Baker J (1946) The histochemical recognition of lipine. Q J Microsc Sci 87:441–4470
Balashov Y (1983) The female reproductive system. In: Balashov YS (ed) An atlas of ixodid tick ultrastructure. Entomological Society of America, Russia, pp 98–128
Bechara GH, Szabó JM, Ferreira B, Garcia M (1995) Rhipicephalus sanguineus tick in Brazil: feeding and reproductive aspects under laboratorial conditions. Braz J Vet Parasitol 4:61–66
Borges A, Cavasin G, Silva I et al (2004) Mortalidade e alterações morfológicas provocadas pela ação inibidora do diflubenzuron na ecdise de larvas de Aedes aegypti (Diptera, Culicidae). Rev Patol Trop 33:91–104
Carvalho HF, Recco-Pimentel SM (2012) A Célula, 3a edn. Editora Manole, São Paulo
Corbel V, Duchon S, Zaim M, Hougard JM (2004) Dinotefuran: a potential neonicotinoid insecticide against resistant mosquitoes. J Med Entomol 41:712–7
Coutinho MTZ, Bueno LL, Sterzik A et al (2005) Participation of Rhipicephalus sanguineus (Acari: Ixodidae) in the epidemiology of canine visceral leishmaniasis. Vet Parasitol 128:149–155. doi:10.1016/j.vetpar.2004.11.011
Craig T (1990) Infectious diseases of the dog and cat. W.B. Saunders Co, Philadelphia
Crampton A, Baxter G, Barker S (1999) Identification and characterisation of a cytochrome P450 gene and processed pseudogene from an arachnid: the cattle tick, Boophilus microplus. Insect Biochem Mol Biol 29:377–384. doi:10.1016/S0965-1748(99)00013-2
Davey RB, Ahrens EH, George JE et al (1998) Therapeutic and persistent efficacy of fipronil against Boophilus microplus (Acari: Ixodidae) on cattle. Vet Parasitol 74:261–276
Denardi SE, Bechara GH, de Oliveira PR et al (2004) Morphological characterization of the ovary and vitellogenesis dynamics in the tick Amblyomma cajennense (Acari: Ixodidae). Vet Parasitol 125:379–95. doi:10.1016/j.vetpar.2004.07.015
Denardi SE, Bechara GH, de Oliveira PR, Camargo-Mathias MI (2010) Azadirachta indica A. Juss (neem) induced morphological changes on oocytes of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick females. Exp Parasitol 126:462–70. doi:10.1016/j.exppara.2010.05.017
Dryden MW, Payne PA, Vicki SR, Kobuszewski D (2011) Efficacy of topically applied dinotefuran formulations an orally administered spinosad tablets against the KS1 Flea strain infesting dogs. Int J Appl Res Vet Med 9:124–129
EPA (2009) Pesticides and toxic substances: pesticide fact sheet dinotefuran. EPA PC Code 044312. www.epa.gov/ opprd001/factsheets/dinotefuran.pdf. Accessed 1 Mar 2009
French TW, Harvey JW (1983) Serologic diagnosis of infectious cyclic thrombocytopenia in dogs using an indirect fluorescent antibody test. Am J Vet Res 44:2407–2411
Friesen KJ, Kaufman WR (2003) Cypermethrin inhibits egg development in the ixodid tick, Amblyomma hebraeum. Pestic Biochem Physiol 76:25–35. doi:10.1016/S0048-3575(03)00032-4
Friesen KJ, Suri R, Kaufman WR (2003) Effects of the avermectin, MK-243, on ovary development and salivary gland degeneration in the ixodid tick, Amblyomma hebraeum. Pestic Biochem Physiol 76:82–90. doi:10.1016/S0048-3575(03)00070-1
González A, D del Castro C, González S (2004) Ectoparasitic species from Canis familiaris (Linné) in Buenos Aires province, Argentina. Vet Parasitol 120:123–9. doi:10.1016/j.vetpar.2003.12.001
Harrison W, Foelix R (1999) Chelicerata: Arthropoda. In: Harrison W, Foelix R (eds) Microscopic anatomy of invertebrates. Wiley-Liss, New York, NY
Hilton H (1982) Biology of insect egg shells. Pergamon, Oxford
Junqueira LC, Carneiro J (2013) Histologia Básica. Guanabara Koogan, Rio de Janeiro
Junqueira LCU, Junqueira LMMS (1983) Técnicas básicas de citologia e histologia. Livraria Editora Santos, São Paulo
Kagabu S (1997) Chloronicotinyl insecticides—discovery, application and future perspective. Rev Toxicol 1:75–129
Kang R, Tang D, Lotze MT, Zeh HJ (2011) RAGE regulates autophagy and apoptosis following oxidative injury. Autophagy 7:442–444
King RC, Vanoucek EG (1960) Oogenesis in adult Drosophila melanogaster. X. Studies on the behavior of the follicle cells. Growth 24:333–338
Kiriyama K, Nishimura K (2002) Structural effects of dinotefuran and analogues in insecticidal and neural activities. Pest Manag Sci 58:669–676. doi:10.1002/ps.493
Koh K, Mori T, Shiraishi S, Uchida TA (1991) Ultrastructural changes of the midgut epithelial cells in feeding and moulting nymphs of the tick Haemaphysalis longicornis. Int J Parasitol 21:23–36
Labruna M, Pereira M (2001) Carrapato em Cães no Brasil. Clín Vet 30:24–32
Lemos WP, Medeiros RS, Zanuncio JC, Serrão JE (2005) Effect of sub-lethal concentrations of permethrin on ovary activation in the predator Supputius cincticeps (Heteroptera: Pentatomidae). Braz J Biol 65:287–290. doi:10.1590/S1519-69842005000200012
Linardi PM, Nagem RL (1973) Pulicídeos e outros ectoparasitos de cães de Belo Horizonte e municípios vizinhos. Rev Bras Biol 33:529–538
McManus JFA (1948) Histological and histochemical uses of periodic acid. Stain Technol 23:99–108
Merle C, Sotto A, Barbuat C, Jourdan J (1998) Disease course of Mediterranean Spotted Fever: remark on 16 cases. In: 7e Colloque sur le Controle Epidemiologique des Maladies Infectieuses. pp 400–401
Nauen R, Bretschneider T (2002) New modes of action of insecticides. Pestic Outlook 13:241–245. doi:10.1039/b211171n
Nodari EF, Roma GC, Furquim KCS et al (2011) Cytotoxic effects of permethrin in salivary glands of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females. Exp Parasitol 128:151–158. doi:10.1016/j.exppara.2011.02.003
Nolan J (1985) Mechanisms of resistance to chemicals in arthropod parasites of veterinary importance. Vet Parasitol 18:155–166
Oliveira PR, Bechara GH, Denardi SE et al (2005) Morphological characterization of the ovary and oocytes vitellogenesis of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 110:146–156. doi:10.1016/j.exppara.2004.12.016
Oliveira PR, Camargo-Mathias MI, Bechara GH (2006) Amblyomma triste (Koch, 1844) (Acari: Ixodidae): morphological description of the ovary and of vitellogenesis. Exp Parasitol 113:179–185. doi:10.1016/j.exppara.2006.01.012
Oliveira PR, Camargo-Mathias MI, Bechara GH (2007) Vitellogenesis in the tick Amblyomma triste (Koch, 1844) (Acari: Ixodidae) Role for pedicel cells. Vet Parasitol 143:134–139. doi:10.1016/j.vetpar.2006.08.013
Oliveira PR, Bechara GH, Camargo-Mathias MI (2008) Evaluation of cytotoxic effects of fipronil on ovaries of semi-engorged Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick female. Food Chem Toxicol 46:2459–2465. doi:10.1016/j.fct.2008.03.034
Oliveira PR De, Bechara GH, Morales MAM, Mathias MIC (2009) Action of the chemical agent fipronil on the reproductive process of semi-engorged females of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Ultrastructural evaluation of ovary cells. Food Chem Toxicol 47:1255–1264. doi:10.1016/j.fct.2009.02.019
Oliveira PR, Bechara GH, Denardi SE et al (2012) Cytotoxicity of fipronil on mice liver cells. Microsc Res Tech 75:28–35. doi:10.1002/jemt.21018
Oliveira PR, Calligaris IB, Roma GC et al (2013) Fluazuron-induced morphophysiological changes in the cuticle formation and midgut of Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) nymphs. Parasitol Res 112:45–58. doi:10.1007/s00436-012-3103-7
Pearse A (1985) Histochemistry theoretical and applied. Livingstone, Churchill
Pruett JH (1999) Immunological control of arthropod ectoparasites—a review. Int J Parasitol 29:25–32. doi:10.1016/S0020-7519(98)00172-6
Remedio RN, Sampieri BR, Vendramini MCR et al (2013) Morphology of the midgut of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) adult ticks in different feeding stages. Parasitol Res 112:415–425. doi:10.1007/s00436-012-3153-x
Roma GC, Furquim KCS, Bechara GH, Camargo-Mathias MI (2010) Permethrin-induced morphological changes in oocytes of Rhipicephalus sanguineus (Acari: Ixodidae) semi-engorged females. Food Chem Toxicol 48:825–830. doi:10.1016/j.fct.2009.12.016
Saito KC, Bechara GH, Nunes ET et al (2005) Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Vet Parasitol 129:299–311. doi:10.1016/j.vetpar.2004.09.020
Sayah F, Fayet C, Idaomar M, Karlinsky A (1996) Effect of Azadirachtin on vitellogenesis of Labidura riparia (Insect Dermaptera). Tissue Cell 28:741–749. doi:10.1016/S0040-8166(96)80077-2
Scudeler EL, Santos DC (2013) Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron 44:125–132. doi:10.1016/j.micron.2012.05.009
Scudeler EL, Padovani CR, Dos Santos DC (2014) Effects of neem oil (Azadirachta indica A. Juss) on the replacement of the midgut epithelium in the lacewing Ceraeochrysa claveri during larval-pupal metamorphosis. Acta Histochem 116:771–780. doi:10.1016/j.acthis.2014.01.008
Sexton DJ, Burgdorfer W, Thomas L, Norment BR (1976) Rocky Mountain spotted fever in Mississippi: survey for spotted fever antibodies in dogs and for spotted fever group Rickettsiae in dog ticks. Am J Epidemiol 103:192–197
Soares AO, Souza AD, Feliciano EA et al (2006) Evaluation of ectoparasites and hemoparasites in dogs kept in apartments and houses with yards in the city of Juiz de Fora, Minas Gerais, Brazil. Rev Bras Parasitol Vet 15:13–6
Sonenshine DE (1991) The female reproductive system. In: Sonenshine DE (ed) Biology of Ticks. Oxford University Press, New York, pp 280–304
Stephen S, Chandrashekara I, Rao KN (1980) Natural occurrence of Coxiella burnetii in the brown dog tick Rhipicephalus sanguineus. Indian J Med Res 71:865–869
Szabó MP, Cunha TM, Pinter A, Vicentini F (2001) Ticks (Acari: Ixodidae) associated with domestic dogs in Franca region, São Paulo, Brazil. Exp Appl Acarol 25:909–16. doi:10.1023/A:1020433003028
Till WM (1961) A contribution to the anatomy and histology of the brown ear tick Rhipicephalus appendiculatus Neumann. Mem Entomol Soc S Afr 6:1–124
Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–68. doi:10.1146/annurev.pharmtox.45.120403.095930
Uneme H, Iwanaga K, Higuchi N et al (1999) Synthesis and insecticidal activity of nitroguanidine derivatives. Pestic Sci 55:202–205. doi:10.1002/(SICI)1096-9063(199902)55:2%3<202::AID-PS869>3.0.CO;2-G
Valotto CFB, Da Silva HHG, Cavasin G et al (2011) Alterações ultraestruturais em larvas de Aedes aegypti submetidas ao diterpeno labdano, isolado de Copaifera reticulata (Leguminosae), e à uma fração rica em taninos de Magonia pubescens (Sapindaceae). Rev Soc Bras Med Trop 44:194–200. doi:10.1590/S0037-86822011005000010
Vendramini MCR, Camargo-Mathias MI, Faria AU et al (2012) Cytotoxic effects of andiroba oil (Carapa guianensis) in reproductive system of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females. Parasitol Res 111:1885–1894. doi:10.1007/s00436-012-3031-6
Wakita T (2011) Molecular design of dinotefuran with unique insecticidal properties. J Agric Food Chem 59:2938–2942. doi:10.1021/jf1030778
Wakita T, Kinoshita K, Yamada E et al (2003) The discovery of dinotefuran: a novel neonicotinoid. Pest Manag Sci 59:1016–1022. doi:10.1002/ps.727
Wakita T, Yasui N, Yamada E, Kishi D (2005) Development of a novel insecticide, dinotefuran. J Pestic Sci 30:133–138. doi:10.1584/jpestics.30.133
Walker AR, Fletcher JD (1987) Histology of digestion in nymphs of Rhipicephalus appendiculatus fed on rabbits and cattle naive and resistant to the ticks. Int J Parasitol 17:1393–1411
Walker JB, Keirans JE, Horak IG (2000) The genus Rhipicephalus (Acari: Ixodidae). A guide to the brown ticks of the world. Cambridge University Press, London
Wall R, Shearer D (1997) Veterinary entomology. Chapman and Hall, London
Watermann BT, Albanis TA, Dagnac T et al (2013) Effects of methyltestosterone, letrozole, triphenyltin and fenarimol on histology of reproductive organs of the copepod Acartia tonsa. Chemosphere 92:544–554. doi:10.1016/j.chemosphere.2013.03.053
Woldehiwet Z, Ristic M (1993) Rickettsial and chlamydial diseases of domestic animals. Pergamon, Oxford
Yoshinari NH, Barros PJL, Bonoldi VLN et al (1997) Perfil da borreliose de Lyme no Brasil. Rev do Hosp das Clínicas da Fac Med São Paulo 52:111–117
Zaim M, Guillet P (2002) Alternative insecticides: an urgent need. Trends Parasitol 18:161–163. doi:10.1016/S1471-4922(01)02220-6
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We would like to thank to CNPQ for financial support, PNPD for financial support, and CNPQ academic career research fellowship to G.H. Bechara and M.I. Camargo-Mathias.
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de Oliveira, P.R., Remédio, R.N., Bechara, G.H. et al. Dinotefuran-induced morphophysiological changes in the ovaries and midgut of semi-engorged females Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) ticks. Parasitol Res 115, 829–849 (2016). https://doi.org/10.1007/s00436-015-4814-3
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DOI: https://doi.org/10.1007/s00436-015-4814-3