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Evaluation of Tagetes patula (Asteraceae) as an ecological alternative in the search for natural control of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae)

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Abstract

The cattle tick Rhipicephalus microplus is a great sanitary problem and causes huge losses to livestock, being a vector of important diseases. The aim of this work was to verify the action of plant-derived material obtained from Tagetes patula on the life cycle of R. microplus, as well as to analyze the action of these extracts on ovary cells of engorged females. In the Adult Immersion Test, the crude ethanolic extract (TpEtOH) showed an efficacy of 99.2% (LC50 = 18.60 mg mL−1). From the repellency test, it was found that both the TpEtOH and essential oil were 100% efficient on the larval stage. In addition, in the Larval Package Test, a mortality of 98.37% was obtained with TpEtOH (LC50 = 3.798 mg mL−1). From the microscopic analysis of ovary cells, morphological changes in the chorion and cytoplasm of oocytes were observed, with vacuolization around the germinal vesicle and disorganization of the pedicular cells, suggesting an interference in the normal embryogenic formation of the larvae. These results demonstrate that T. patula extracts interfere at all stages of development of the ixodid, from eggs to adults forms, and have a pronounced repellent effect. In addition, the results of the cytotoxicity assays performed on keratinocytes, as well as previous information on oral and dermal acute toxicity (LD50 > 4000 mg kg−1), attest that T. patula can be a safe alternative for ectoparasitic control, representing an alternative for development of a formulation used to help control populations of ticks in the field.

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References

  • Almeida MB, Tortelli FPY, Rietcorrea B, Ferreira JLM, Soares MP, Farias NAR, Riet-Correa F, Schild AL (2006) Tristeza parasitária bovina na região sul do Rio Grande do Sul: estudo retrospectivo de 1978 a 2005. Pesq Vet Bras 26(4):237–242

    Article  Google Scholar 

  • Arnosti A, Brienza PD, Furquim KCS, Chierice GO, Neto SC, Bechara GH, Sampieri BR, Camargo-Mathias MI (2011) Effects of Ricinus communis oil esters on salivary glands of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 127(2):569–574

    Article  CAS  PubMed  Google Scholar 

  • Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58:1–30

    Article  CAS  Google Scholar 

  • Balashov YS (1972) Bloodsucking ticks (Ixodoidea)—Vector of diseases of man and animals. Misc Publ Entomol Soc Am 8:1–376

    Google Scholar 

  • Barros ATM, Gomes A, Koller WW (2007) Insecticide susceptibility of horn flies, Haematobia irritans (Diptera: Muscidae), in the state of Mato Grosso do Sul. Brazil. Rev Bras Parasitol Vet 16(3):145–151

    Article  PubMed  Google Scholar 

  • Castro KNC, Lima DF, Vasconcelos LC, Leite JRSA, Santos RC, Paz Neto AA, Costa-Júnior LM (2014) Acaricide activity in vitro of Acmella oleracea against Rhipicephalus microplus. Parasitol Res 113:3697–3701

    Article  CAS  PubMed  Google Scholar 

  • Chagas ACS, Rabelo MD (2012) Método para detecção de substâncias com atividade repelente sobre larvas do carrapato Rhipicephalus (Boophilus) microplus: revisão e recomendações. Documentos Embrapa Pecuária Sudeste 106, São Carlos

  • Chagas ACS, Georgetti CS, Carvalho CO, Oliveira MC, Rodrigues RA, Foglio MA, Magalhães PM (2011) In vitro activity of Artemisia annua L. (Asteraceae) extracts against Rhipicephalus (Boophilus) microplus. Rev Bras Parasitol Vet 20(1):31–35

    Article  PubMed  Google Scholar 

  • Chagas ACS, Leite RC, Furlon J, Prates HT, Passos WM (2003) Sensibilidade do carrapato Boophilus microplus a solventes. Ciênc Rural 33:109–114

    Article  Google Scholar 

  • Denardi SE, Bechara GH, Oliveira PR, Camargo-Mathias MI (2012) Ultrastructural analysis of the oocytes of female Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) ticks subjected to the action of Azadirachta indica A. Juss (Neem). Ultrastruct Pathol 36(1):56–67

    Article  PubMed  Google Scholar 

  • Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and Boophilus microplus: laboratory tests for insecticides. J Econ Entomol 66:130–133

    Article  CAS  PubMed  Google Scholar 

  • FAO (1971) Recommended methods for the detection and measurement of resistance of agricultural pests to pesticides—tentative method for larvae ticks, Boophilus spp., vol. 19. Food and Agriculture Organization, Rome, pp 15–18

  • Felsheim RF, Chávez ASO, Palmer GH, Crosby L, Barbet AF, Kurtti TJ, Munderloh UG (2010) Transformation of Anaplasma marginale. Vet Parasitol 167(2–4):167–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geran RI, Greenberg NH, Macdolnald MM, Schumacher AM, Abbott BJ (1972) Protocols for screening chemical agents and natural products against animal tumors and other biological systems. Cancer Chemother Rep 3:1–103

    Google Scholar 

  • Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, León AAP, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 23(2):150–156

    Article  Google Scholar 

  • Guedes-Junior DS, Araújo FR, Silva FJM, Rangel CP, Barbosa-Neto JD, Fonseca AH (2008) Frequency of antibodies to Babesia bigemina, B. bovis, Anaplasma marginale, Trypanosoma vivax and Borrelia burdgorferi in cattle from the northeastern region of the state of Pará. Brazil. Rev Bras Parasitol Vet 17:105–109

    Article  Google Scholar 

  • Halket JM, Zaikin VG (2003) Derivatization in mass spectrometry–1. Silylation. Eur J Mass Spectrom 9(1):1–21

    Article  CAS  Google Scholar 

  • Hazari MM, Misra SC (1993) Behaviour and survival of Boophilus microplus larvae under outdoor conditions. Indian Vet J 3(2):187–188

    Google Scholar 

  • Homer MJ, Aguilar-Delfin I, Telford SR III, Krause PJ, Persing DH (2000) Babesiosis. Clin Microbiol Rev 13(3):451–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaenson TGT, Pålsson K, Borg-Karlson AK (2005) Evaluation of extracts and oils of tick-repellent plants from Sweden. Med Vet Entomol 19(4):345–352

    Article  CAS  PubMed  Google Scholar 

  • Jonsson NN, Matschoss AL (1998) Attitudes and practices of Queensland dairy farmers to the control of the cattle tick, Boophilus microplus. Aust Vet J 76(11):746–751

    Article  CAS  PubMed  Google Scholar 

  • Labruna MB, Camargo LMA, Terrassini FA, Ferreira F, Schumaker TTS, Camargo EP (2005) Ticks (Acari: Ixodidae) from the state of Rondônia, western Amazon, Brazil. Syst Appl Acarol 10(1):17–32

    Google Scholar 

  • Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679–2688

    Article  PubMed  PubMed Central  Google Scholar 

  • Mello INK, Silveira WF (2012) Resíduos de agrotóxicos em produtos de origem animal. Acta Vet Bras 6(2):94–104

    Google Scholar 

  • Odhiambo TR (1982) Current themes in tropical science: physiology of ticks. Pergamon, Oxford

    Google Scholar 

  • Pellati F, Benvenuti S (2007) Chromatographic and electrophoretic methods for the analysis of phenetylamine alkaloids in Citrus aurantium. J Chromatogr A 1161(1–2):71–88

    Article  CAS  PubMed  Google Scholar 

  • Politi FAS, Figueira GM, Araújo AM, Sampieri BR, Camargo-Mathias MI, Szabó MPJ, Bechara GH, Dos Santos LC, Vilegas W, Pietro RCLR (2012) Acaricidal activity of ethanolic extract from aerial parts of Tagetes patula L. (Asteraceae) against larvae and engorged adult females of Rhipicephalus sanguineus (Latreille, 1806). Parasit Vectors 5:295–306

    Article  PubMed  PubMed Central  Google Scholar 

  • Politi FAS, Souza-Moreira TM, Rodrigues ER, Queiroz-Fernandes GM, Figueira GM, Januário AH, Berenger JM, Socolovschi C, Parola P, Pietro RCLR (2013) Chemical characterization and acaricide potential of essential oil from aerial parts of Tagetes patula L. (Asteraceae) against engorged adult females of Rhipicephalus sanguineus (Latreille, 1806). Parasitol Res 112:2261–2268

    Article  PubMed  Google Scholar 

  • Politi FAS, Figueira GM, Camargo-Mathias MI, Berenger JM, Parola P, Pietro RCLR (2015) Action of ethanolic extract from aerial parts of Tagetes patula L. (Asteraceae) on hatchability and embryogenesis of Rhipicephalus sanguineus eggs (Acari: Ixodidae). Ind Crops Prod 67:55–61

    Article  CAS  Google Scholar 

  • Politi FAS, Queiroz-Fernandes GM, Rodrigues ER, Freitas JA, Pietro RCLR (2016) Antifungal, antiradical and cytotoxic activities of extractives obtained from Tagetes patula L. (Asteraceae), a potential acaricide plant species. Microb Pathog 95:15–20

    Article  PubMed  Google Scholar 

  • Politi FAS, Nascimento JD, Silva AA, Moro IJ, Garcia ML, Guido RVC, Pietro RCLR, Godinho AF, Furlan M (2017) Insecticidal activity of an essential oil of Tagetes patula L. (Asteraceae) on common bed bug Cimex lectularius L. and molecular docking of major compounds at the catalytic site of ClAChE1. Parasitol Res 116(1):415–424

    Article  PubMed  Google Scholar 

  • Roma GC, Furquim KC, Bechara GH, Camargo-Mathias MI (2010) Permethrin-induced morphological changes in oocytes of Rhipicephalus sanguineus (Acari: Ixodidae) semi-engorged females. Food Chem Toxicol 48(3):825–830

    Article  CAS  PubMed  Google Scholar 

  • Roma GC, Furquim KC, Bechara GH, Camargo-Mathias MI (2011) Cytotoxic effects of permethrin in oocytes of Rhipicephalus sanguineus (Acari: Ixodidae) fully engorged females: I. Direct or indirect action of the acaricide in germ cells? Exp Appl Acarol 53(3):287–299

    Article  CAS  PubMed  Google Scholar 

  • Roy BC, Krucken J, Ahmed JS, Majumder S, Baumann MP, Clausen PH, Nijhof AM (2017) Molecular identification of tick-borne pathogens infecting cattle in Mymensingh district of Bangladesh reveals emerging species of Anaplasma and Babesia. Transbound Emerg Dis 00:1–12

    Google Scholar 

  • Saito KC, Bechara GH, Nunes ET, Oliveira PR, Denardi SE, Camargo-Mathias MI (2005) Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Vet Parasitol 129(3–4):299–311

    Article  Google Scholar 

  • Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82(13):1107–1112

    Article  CAS  Google Scholar 

  • Soares JF, Sangioni LA, Vogel FSF, Silva FB (2007) Parasitismo em ser humano por B. microplus (Acari: Ixodidae) em Santa Maria, RS, Brasil. Ciênc Rural 37(5):1495–1497

    Article  Google Scholar 

  • Sonenshine DE (1991) Biology of ticks. Oxford University Press, Oxford

    Google Scholar 

  • Steullet P, Guerin PM (1994) Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae). I. Receptors within the Haller’s organ capsule. J Comp Physiol A 174(1):27–38

    Article  CAS  PubMed  Google Scholar 

  • Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1998) Parasitologia Veterinária. Guanabara-Koogan, Rio de Janeiro

    Google Scholar 

  • USDA (2014) United States Department of Agriculture, Foreign Agricultural Service. https://apps.fas.usda.gov/psdonline/app/index.html#/app/home. Accessed 14 Mar 2018

  • Van den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr 11:463–471

    Article  Google Scholar 

  • Vannier E, Krause PJ (2009) Update on babesiosis. Interdiscip Perspect Infect Dis 2009:984568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vendramini MCR, Camargo-Mathias MI, De Faria AU, Furquim KCS, De Souza LP, Bechara GH, Roma GC (2012) Action of andiroba oil (Carapa guianensis) on Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females: morphophysiological evaluation of reproductive system. Microsc Res Tech 75(12):1745–1754

    Article  CAS  PubMed  Google Scholar 

  • Yunes RA, Pedrosa RC, Cechinel-Filho V (2001) Fármacos e fitoterápicos: a necessidade do desenvolvimento da indústria de fitoterápicos e fitofármacos no Brasil. Quím Nova 24(1):147–152

    Article  CAS  Google Scholar 

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Acknowledgements

FASP and MF thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, process number 2013/03493-8 and process number 2013/07600-3/CIBFar) and the National Council of Technological and Scientific Development (CNPq, process number 150302/2017-7) for research fellowships. We thank the Embrapa Project No. 02.13.01.001.00-00 for the financial support to maintain the tick donors and to perform in vitro tick assays. We also thank the Collection of Medicinal and Aromatic Plants (CPMA) of the Multidisciplinary Center for Chemical, Biological and Agricultural Research (CPQBA) for supplying the plant material; Prof. Norberto Peporine Lopes of the Research Support Center in Natural and Synthetic Products (NPPNS), Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo (USP), for providing the chromatographic equipment; and Prof. Dr. Christiane Pienna Soares of the Laboratory of Cytology and Cell Biology (UNESP), Araraquara (SP), for providing the HaCat cells.

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Politi, F.A.S., Fantatto, R.R., da Silva, A.A. et al. Evaluation of Tagetes patula (Asteraceae) as an ecological alternative in the search for natural control of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Exp Appl Acarol 77, 601–618 (2019). https://doi.org/10.1007/s10493-019-00368-2

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