Seasonal analysis and acaricidal activity of the thymol-type essential oil of Ocimum gratissimum and its major constituents against Rhipicephalus microplus (Acari: Ixodidae)

Abstract

The tick Rhipicephalus microplus affects cattle health, with production loss in tropical and subtropical regions. Moreover, the use of commercial acaricides has been reduced due to the resistance of this parasite. Although alternatives such as plant bioactive molecules have been sought, essential oils present variations in their chemical constituents due to environmental factors, which can interfere with their acaricidal activity. The objective of the present study was to evaluate the seasonal influence of the essential oil of Ocimum gratissimum and its major constituents on acaricidal activity against R. microplus larvae. A high-yield essential oil of O. gratissimum and its major constituents were used, and a plant with a thymol-type oil was selected for seasonal analysis and acaricidal activity against R. microplus. Gas chromatography (GC) and GC-mass spectrometry (MS) were employed to identify 31 oil constituents (average yield of 6.26%). The main compounds were found to be thymol (33.4 to 47.9%), γ-terpinene (26.2 to 36.8%), and p-cymene (4.3 to 17.0%). Concerning acaricidal activity, the December (LC50 0.84 mg/mL) and September (LC50 1.58 mg/mL) oils obtained in the dry season were the most active, and assays performed with commercial standards revealed LC50 values of p-cymene, thymol, and γ-terpinene of 1.41, 1.81, and 3.08 mg/mL, respectively. Overall, lower acaricidal activities were found for oils produced from plants harvested in the rainy season. The results showed that seasonal variation in the chemical composition of the O. gratissimum essential oil influences its acaricidal activity. The seasonal variations in the thymol-type essential oil of O. gratissimum can represent an important strategy for the control of R. microplus.

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References

  1. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Publ. Corp, Carol Stream, IL, USA

    Google Scholar 

  2. Adebolu TT, Oladimeji SA (2005) Antimicrobial activity of leaf extracts of Ocimum gratissimum on selected diarrhea causing bacteria in southwestern Nigeria. Afr J Biotechnol 4:682–684

    Article  Google Scholar 

  3. Araújo LX, Novato TPL, Zeringota V, Matos RS, Senra TOS, Maturano R, Prata MCA, Daemon E, Monteiro CMO (2015) Acaricidal activity of thymol against larvae of Rhipicephalus microplus (Acari: Ixodidae) under semi-natural conditions. Parasitol Res 114:3271–3276

    Article  PubMed  Google Scholar 

  4. Banumathi B, Vaseeharan B, Rajasekar P, Prabhu NM, Ramasamy P, Murugan K, Canale A, Benelli G (2017) Exploitation of chemical, herbal and nanoformulated acaricides to control the cattle tick, Rhipicephalus (Boophilus) microplus—a review. Vet Par 244:101–110

    Article  Google Scholar 

  5. Benelli G, Pavela R, Canale A, Mehlhorn H (2016) Tick repellents and acaricides of botanical origin: a green roadmap to control tick-borne diseases? Parasitol Res 115:2545–2560

    Article  PubMed  Google Scholar 

  6. Benitez NP, León EMM, Stashenko EE (2009) Eugenol and methyl eugenol chemotypes of essential oil of species Ocimum gratissimum L. and Ocimum campechianum Mill. from Colombia. J Chromatogr Sci 47:800–803

    CAS  Article  Google Scholar 

  7. Blank AF, Sant’ana TCP, Santos PS, Arrigoni-Blank MF, Prata APN, Jesus HCR, Alves PB (2011) Chemical characterization of the essential oil from patchouli accessions harvested over four seasons. Ind Crops Prod 34:831–837

    CAS  Article  Google Scholar 

  8. Borugã O, Jianu C, Miscã C, Golet I, Gruia AT, Horhat FG (2014) Thymus vulgaris essential oil: chemical composition and antimicrobial activity. J Med Life 7:56–60

    PubMed  PubMed Central  Google Scholar 

  9. Castro JAM (2015) Avaliação sazonal, circadiana, antifúngica e antioxidante do óleo essencial de Ocimum gratissimum L. (Alfavaca). Dissertação de Mestrado, Programa de Pós-Graduação em Química, Universidade Federal do Maranhão, 73 p

  10. Cetin H, Cilek JE, Aydin L, Deveci O, Yanikoglu A (2010) Acaricidal activity of Satureja thymbra L. essential oil and its major components, carvacrol and γ-terpinene against adult Hyalomma marginatum (Acari: Ixodidae). Vet Parasitol 170:287–290

    CAS  Article  PubMed  Google Scholar 

  11. Costa-Junior LM, Miller RJ, Alves PB, Blank AF, Li AY, León AAP (2016) Acaricidal efficacies of Lippia gracilis essential oil and its phytochemicals against organophosphate-resistant and susceptible strains of Rhipicephalus (Boophilus) microplus. Vet Parasitol 228:60–64

    CAS  Article  PubMed  Google Scholar 

  12. Cruz EMO, Costa-Junior LM, Pinto JAO, Santos DA, Araujo SA, Arrigoni-Blank MF, Bacci L, Alves PB, Cavalcanti SCH, Blank AFG (2013) Acaricidal activity of Lippia gracilis essential oil and its major constituents on the tick Rhipicephalus (Boophilus) microplus. Vet Parasitol 195:198–202

    Article  PubMed  Google Scholar 

  13. Cruz EMO, Pinto JAO, Fontes SS, Arrigoni-Blank MF, Bacci L, Jesus HCR, Santos DA, Alves PB, Blank AF (2014) Water deficit and seasonality study on essential oil constituents of Lippia gracilis Schauer germplasm. Sci World J:1–9

  14. Daemon E, Monteiro CMO, Rosa LS, Clemente MA, Arcoverde A (2009) Evaluation of the acaricide activity of thymol on engorged and unengorged larvae of Rhipicephalus sanguineus (Latreille, 1808) (Acari: Ixodidae). Parasitol Res 105:495–497

    Article  PubMed  Google Scholar 

  15. Dubey NK, Tiwari TN, Mandin D, Adriamboavonjy H, Chaumount JP (2000) Antifungal properties of Ocimum gratissimum essential oil (ethyl cinnamate chemotype). Fitoterapia 71:567–569

    CAS  Article  PubMed  Google Scholar 

  16. Ennajar M, Afloulous S, Romdhane M, Ibrahim H, Cazaux S, Abderraba M, Raies A, Bouajila J (2011) Influence of the process, season, and origin on volatile composition and antioxidant activity of Juniperus phoenicea L. leaves essential oils. J Food Sci 76(2):C224–C230

  17. Evergetis E, Michaelakis A, Papachristos DP, Badieritakis E, Kapsaski-Kanelli VN, Haroutounian SA (2016) Seasonal variation and bioactivity of the essential oils of two Juniperus species against Aedes (Stegomyia) albopictus (Skuse, 1894). Parasitol Res 115(6):2175–2183

    CAS  Article  PubMed  Google Scholar 

  18. FAO, (2004). Resistance management and integrated parasite control in ruminants. Guidelines. (Available in: <http://www.fao.org/ag/aga.html>)

  19. Faria TJ, Ferreira RS, Yassumoto L, Souza JRP, Ishikawa NK, Barbosa AM (2006) Antifungal activity of essential oil isolated from Ocimum gratissimum L. (eugenol chemotype) against phytopathogenic fungi. Braz Arch Biol and Technol 49:867–871

    CAS  Article  Google Scholar 

  20. Figueiredo AC, Barroso JG, Pedro LG, Scheffer JJC (2008) Factors affecting secondary metabolite production in plants: volatile components and essential oils. Flav Fragr J 23:213–226

    CAS  Article  Google Scholar 

  21. Freire CMM, Marques MOM, Costa M (2006) Effects of seasonal variation on the central nervous system activity of Ocimum gratissimum L. essential oil. J Ethnopharmacol 105:161–166

    CAS  Article  PubMed  Google Scholar 

  22. Graf JF, Gogolewski R, Leach-Bing N, Sabatini GA, Bordin EL, Arantes GJ (2004) Tick control: an industry point of view. Parasitology 129:427–442

    Article  Google Scholar 

  23. Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, Leon AAP, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Braz J Vet Parasitol 23:15–156

    Google Scholar 

  24. Hue T, Cauquil L, Hzounda FJB, Jazet DP, Bakarnga-Via I, Menut C (2015) Acaricidal activity of five essential oils of Ocimum species on Rhipicephalus (Boophilus) microplus larvae. Parasitol Res 114:91–99

    CAS  Article  PubMed  Google Scholar 

  25. Kéita SM, Vincent C, Schmit JP, Arnason JT, Bélanger A (2001) Efficacy of essential oil of Ocimum basilicum L. and O. gratissimum L. applied as an insecticidal fumigant and powder to control Callosobruchus maculatus (Fab.) [Coleoptera: Bruchidae]. J Stored Prod Res 37:339–349

    Article  PubMed  Google Scholar 

  26. Kiazolu JB, Intisar A, Zhang L, Wang Y, Zhang R, Wu Z, Zhang W (2016) Phytochemical screening and chemical variability in volatile oils of aerial parts of Morinda morindoides. Nat Prod Res 30:2249–2252

    CAS  Article  PubMed  Google Scholar 

  27. Klafke GM, Sabatini GA, Albuquerque TA, Martins JR, Kemp DH, Miller RJ, Schumaker TTS (2006) Larval immersion tests with ivermectin in populations of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) from state of São Paulo, Brazil. Vet Parasitol 142:386–390

    CAS  Article  PubMed  Google Scholar 

  28. Koba K, Poutouli PW, Raynaud C, Sanda K (2009) Antifungal activity of the essential oils from Ocimum gratissimum L. grown in Togo. J. Sci Res 1:164–171

    CAS  Google Scholar 

  29. Krstev TM, Radnovic D, Kilic D, Zlatkovic B, Ristic M, Brankovic S (2009) Chemical composition and antimicrobial activity of Satureja hortensis L. essential oil. Cent Eur J Biol 4:411–416

    Google Scholar 

  30. Kumar S, Sharma AK, Nagar G, Ghosh S (2015) Determination and establishment of discriminating concentrations of malathion, coumaphos, fenvalerate and fipronil for monitoring acaricide resistance in ticks infesting animals. Ticks Tick Borne Dis 6:383–387

    Article  PubMed  Google Scholar 

  31. Lage TC, Montanari RM, Fernandes SA, Oliveira Monteiro CM, Souza O, Senra T, Zeringota V, Calmon F, Matos RS, Daemon E (2013) Activity of essential oil of Lippia triplinervis Gardner (Verbenaceae) on Rhipicephalus microplus (Acari: Ixodidae). Parasitol Res 112:863–869

    Article  PubMed  Google Scholar 

  32. Lem MF, Payne VK, Poné JW, Jeannette Y, Tayo GM, Tchoumboué J (2014) In vitro ovicidal and larvicidal activities of stem bark of Terminalia glaucescens (Combretaceae) against Haemonchus contortus. Am J Plant Sci 5:2859–2868

    Article  Google Scholar 

  33. Lima AS, Carvalho JF, Peixoto MG, Blank AF, Borges LMF, Costa Junior LM (2016) Assessment of the repellent effect of Lippia alba essential oil and major monoterpenes on the cattle tick Rhipicephalus microplus. Med Vet Entomol 30:73–77

    Article  Google Scholar 

  34. Maffei ME (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bo 76:612–631

    CAS  Article  Google Scholar 

  35. Maia JGS, Zoghbi MGB, Andrade EHA (2001) Plantas aromáticas na Amazônia e seus óleos essenciais. Coleção Adolpho Ducke, Museu Paraense Emilio Goeldi, Belém 173p

    Google Scholar 

  36. Medini H, Elaissi A, Farhat F, Khouja ML, Chemli R, Harzallah-Skhiri F (2009) Seasonal and geographical influences on the chemical composition of Juniperus phoenicea L. essential oil leaves from the Northern Tunisia. Chem Biodivers 6(9):1378–1387

  37. Mossi AJ, Pauletti GF, Rota L, Echeverrigaray S, Barros IBI, Oliveira JV, Paroul N, Cansian RL (2012) Effect of different liming levels on the biomass production and essential oil extraction yield of Cunila galioides Benth. Braz J Biol 72:787–793

    CAS  Article  PubMed  Google Scholar 

  38. Nist - National Institute of Standards and Technology (2005) Mass spectral library (Nist/Epa/Nih, v. 2.0d). The NIST Mass Spectrometry Data Center, Gaithersburg

  39. Pandey AK, Singh P, Tripathi NN (2014) Chemistry and bioactivities of essential oils of some Ocimum species: an overview. Asian Pac J Trop Biomed 4:682–694

    CAS  Article  Google Scholar 

  40. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21(12):1000–1007

    CAS  Article  PubMed  Google Scholar 

  41. Pavela R, Canale A, Mehlhorn H, Benelli G (2016) Application of ethnobotanical repellents and acaricides in prevention, control and management of livestock ticks: a review. Res Vet Sci 109:1–9

    Article  PubMed  Google Scholar 

  42. Peixoto MG, Costa-Júnior LM, Blank AF, Lima AS, Menezes TSA, Santos DA, Alves PB, Cavalcante SCH, Bacci L, Arrigoni-Blank MF (2015) Acaricidal activity of essential oils from Lippia alba genotypes and its major components carvone, limonene, and citral against Rhipicephalus microplus. Vet Parasitol 210:118–122

    CAS  Article  PubMed  Google Scholar 

  43. Piątkowska E, Rusiecka-Ziółkowska J (2016) Influence of essential oils on infectious agents. Adv Clin Exp Med 25:989–995

    Article  PubMed  Google Scholar 

  44. Poulose AJ, Croteau R (1978) γ-Terpinene synthetase: a key enzyme in the biosynthesis of aromatic monoterpenes. Arch Biochem Biophys 191:400–411

    CAS  Article  PubMed  Google Scholar 

  45. Reck J, Klafke GM, Dall’Agnol B, Scheffer R, Souza UA, Corassini VB, Vargas R, Santos JS, Martins JR (2014) First report of fluazuron resistance in Rhipicephalus microplus: a field tick population resistant to six classes of acaricides. Vet Parasitol 17:128–136

    Article  Google Scholar 

  46. Roditakis E, Roditakis NE, Tsagkarakou A (2005) Insecticide resistance in Bemisia tabaci (Homoptera: Aleyrodidae) populations from Crete. Pest Manag Sci 61:577–582

    CAS  Article  PubMed  Google Scholar 

  47. Sampaio BL, Edrada-Ebel R, Costa FB (2016) Effect of the environment on the metabolic profile of Tithonia diversifolia: a model for environmental metabolomics of plants. Sci Rep 6:1–11

    Article  Google Scholar 

  48. Santos CP, Pinto JAO, Santos CA, Cruz EMO, Arrigoni-Blank MF, Andrade TM, Santos DA, Alves PB, Blank AF (2016) Harvest time and geographical origin affect the essential oil of Lippia gracilis Schauer. Ind Crop Prod 79:205–210

    CAS  Article  Google Scholar 

  49. Scolarick MG, Daemon E, Monteiro CMO, Maturano R (2012) Enhancing the acaricide effect of thymol on larvae of the cattle tick Rhipicephalus microplus (Acari: Ixodidae) by solubilization in ethanol. Parasitol Res 110:645–648

    Article  Google Scholar 

  50. Soares AMS, Penha TA, Araújo SA, Cruz EMO, Blank EF, Costa-Junior LM (2016) Assessment of different Lippia sidoides genotypes regarding their acaricidal activity against Rhipicephalus (Boophilus) microplus. Braz J Vet Parasitol 25:401–406

    Article  Google Scholar 

  51. Suhr KI, Nielsen PV (2003) Antifungal activity of essential oils evaluated by two different application techniques against rye bread spoilage fungi. J Appl Microbiol 94:665–674

    CAS  Article  PubMed  Google Scholar 

  52. Tabari MA, Youssefi MR, Maggi F, Benelli G (2017) Toxic and repellent activity of selected monoterpenoids (thymol, carvacrol and linalool) against the castor bean tick, Ixodes ricinus (Acari: Ixodidae). Vet Parasitol 245:86–91

    CAS  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  54. Vieira RF, Grayer RJ, Paton A, Simon JE (2001) Genetic diversity of Ocimum gratissimum L. based on volatile oil constituents, flavonoids and RAPD markers. Biochem Syst Ecol 29:287–304

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank CNPq (The Brazilian National Council for Scientific and Technological Development) for awarding a fellowship to L.M. Costa-Júnior, CAPES (Brazilian Federal Agency for support and evaluation of graduate education) and FAPEMA (Maranhão State Research Foundation) for the scholarships to A.S. Lima and M.N. Milhomem, respectively. We also thank CNPq and FAPEMA for their financial support and Dr. JRS Martins for donating the R. microplus strain.

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Correspondence to Lívio Martins Costa-Junior.

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This study was approved by the UFMA ethics committee, under number 23115018061/2011-01.

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Silva Lima, A., Milhomem, M.N., Santos Monteiro, O. et al. Seasonal analysis and acaricidal activity of the thymol-type essential oil of Ocimum gratissimum and its major constituents against Rhipicephalus microplus (Acari: Ixodidae). Parasitol Res 117, 59–65 (2018). https://doi.org/10.1007/s00436-017-5662-0

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Keywords

  • Natural product
  • Thymol
  • γ-Terpinene
  • p-Cymene
  • Tick
  • Acaricidal activity