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.
Similar content being viewed by others
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
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
Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58:1–30
Balashov YS (1972) Bloodsucking ticks (Ixodoidea)—Vector of diseases of man and animals. Misc Publ Entomol Soc Am 8:1–376
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
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
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
Chagas ACS, Leite RC, Furlon J, Prates HT, Passos WM (2003) Sensibilidade do carrapato Boophilus microplus a solventes. Ciênc Rural 33:109–114
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
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
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
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
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
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
Halket JM, Zaikin VG (2003) Derivatization in mass spectrometry–1. Silylation. Eur J Mass Spectrom 9(1):1–21
Hazari MM, Misra SC (1993) Behaviour and survival of Boophilus microplus larvae under outdoor conditions. Indian Vet J 3(2):187–188
Homer MJ, Aguilar-Delfin I, Telford SR III, Krause PJ, Persing DH (2000) Babesiosis. Clin Microbiol Rev 13(3):451–469
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
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
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
Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679–2688
Mello INK, Silveira WF (2012) Resíduos de agrotóxicos em produtos de origem animal. Acta Vet Bras 6(2):94–104
Odhiambo TR (1982) Current themes in tropical science: physiology of ticks. Pergamon, Oxford
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
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
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
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
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
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
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
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
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
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
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
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
Sonenshine DE (1991) Biology of ticks. Oxford University Press, Oxford
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
Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1998) Parasitologia Veterinária. Guanabara-Koogan, Rio de Janeiro
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
Vannier E, Krause PJ (2009) Update on babesiosis. Interdiscip Perspect Infect Dis 2009:984568
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-019-00368-2