Skip to main content
SpringerLink
Log in

Acaricidal activity of the hexanic and hydroethanolic extracts of three medicinal plants against southern cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae)

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

The southern cattle tick Rhipicephalus microplus is a major problem for the cattle industry in tropical and subtropical areas worldwide. Chemical products are commonly applied to control it; however, their indiscriminate use has resulted in the appearance of resistant lineages. In the last decades, plants have been used as an alternative to conventional acaricidal drugs, as several plant compounds repel activity, decrease the reproductive potential and reduce the survival rate of ticks. For this reason, the in vitro efficacy of hexanic and hydroalcoholic extracts of Randia aculeata, Moringa oleifera and Carica papaya were evaluated against the larvae and engorged females of R. microplus. Larval packet tests and adult immersion tests were performed with seven concentrations of each of the extracts. The extracts obtained with hydroethanolic solution (polar solvent) exhibited a higher acaricidal activity than extracts prepared with n-hexane (non-polar solvent). Hydroethanolic extracts of R. aculeata seed and shell showed the highest larvicidal activity against R. microplus (100 and 91% mortality, respectively) at a concentration of 100 mg/mL. Randia aculeata (seed and shell), M. oleifera and C. papaya treatments at the same concentration (100 mg/mL) also resulted in adult mortality of 85, 75, 66 and 55%, respectively. The adult immersion test showed that hydroethanolic extracts derived from R. aculeata seed significantly reduced the index of egg laying and increased the percentage inhibition of oviposition of female ticks at a concentration of 100 mg/mL. These results indicate that the tested extracts exhibit acaricidal activity and could be considered as potential agents for the development of alternative natural acaricides against R. microplus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Adenubi OT, McGaw LJ, Eloff JN, Naidoo V (2018) In vitro bioassays used in evaluating plant extracts for tick repellent and acaricidal properties: a critical review. Vet Parasitol 254:160–171

    Article  PubMed  Google Scholar 

  • Agra-Neto AC, Napoleão TH, Pontual EV (2014) Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res 113:175–184

    Article  PubMed  Google Scholar 

  • Akhtar Y, Shikano I, Isman MB (2009) Topical application of a plant extract to different life stages of Trichoplusia ni fails to influence feeding or oviposition behavior. Entomol Exp Appl 132:275–282

    Article  Google Scholar 

  • Álvarez-Román R, Silva-Flores PG, Galindo-Rodríguez SA, Huerta-Heredia AA, Vilegas W, Paniagua-Vega D (2020) Moisturizing and antioxidant evaluation of Moringa oleifera leaf extract in topical formulations by biophysical techniques. S African J Bot 129:404–411

    Article  CAS  Google Scholar 

  • Antoun MD, Gerena L, Milhous WK (1993) Screening of the flora of Puerto rico for potential antimalarial bioactives. Pharm Biol 31:255–258

    Google Scholar 

  • Athanasiadou S, Kyriazakis I, Jackson F, Coop RL (2001) Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Vet Parasitol 99:205–219

    Article  CAS  PubMed  Google Scholar 

  • Banumathi B, Vaseeharan B, Rajasekar P, Prabhu NM, Ramasamy P, Murugan K, Benelli G (2017) Exploitation of chemical, herbal and nanoformulated acaricides to control the cattle tick, Rhipicephalus (Boophilus) microplus–a review. Vet Parasitol 244:102–110

    Article  CAS  PubMed  Google Scholar 

  • Bennett GF (1974) Oviposition of Boophilus microplus (Canestrini) (Acarida: Ixodidae). Influence of tick size on egg production. Acarologia 16:52–61

    CAS  PubMed  Google Scholar 

  • Cardoso A, Santos E, Lima A, Temeyer KB, Pérez de León AA, Costa LM (2020) Terpenes on Rhipicephalus (Boophilus) microplus: Acaricidal activity and acetylcholinesterase inhibition. Vet Parasitol. https://doi.org/10.1016/j.vetpar.2020.109090

    Article  PubMed  Google Scholar 

  • Chagas AC, Passos WM, Prates HT, Leite RC, Furlong J, Fortes ICP (2002) Efeito acaricida de óleos essenciais e concentrados emulsionáveis de Eucalyptus spp em Boophilus microplus. Brazilian J Vet Res Anim Sci 39:247–253

    Article  Google Scholar 

  • Chagas AC, Domingues LF, Fantatto RR, Giglioti R, Oliveira MC, Oliveira DH, Mano RA, Jacob RG (2014) In vitro and in vivo acaricide action of juvenoid analogs produced from the chemical modification of Cymbopogon spp. and Corymbia citriodora essential oil on the cattle tick Rhipicephalus (Boophilus) microplus. Vet Parasitol 205:277–284

    Article  CAS  PubMed  Google Scholar 

  • Cherry LM (1969) The production of cuticle wax by engorged females of the cattle tick, Boophilus Microplus (Canestrini). J Exp Biol 50:705–770

    Article  CAS  PubMed  Google Scholar 

  • Coelho JS, Santos NDL, Napoleão TH, Gomes FS, Ferreira RS, Zingali RB, Coelho LCBB, Leite SP, Navarro DMAF, Paiva PMG (2009) Effect of Moringa oleifera lectin on development and mortality of Aedes aegypti larvae. Chemosphere 77:934–938

    Article  CAS  PubMed  Google Scholar 

  • Dawkar VV, Chikate YR, Lomate PR, Dholakia BB, Gupta VS, Giri AP (2013) Molecular insights into resistance mechanisms of lepidopteran insect pests against toxicants. J Proteome Res 12:4727–4737

    Article  CAS  PubMed  Google Scholar 

  • Dougoud J, Toepfer S, Bateman M (2019) Efficacy of homemade botanical insecticides based on traditional knowledge. A Review Agron Sustain Dev 39:37

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ekaiko M, Stephen C, Emmanuel U, Chizaram E (2015) Antimicrobial screening and phytochemical analysis of Carica papaya leaf extracts. Stand Res J Microbiol Sci 2:1–4

    Google Scholar 

  • Estrada-Peña A, Garcia Z, Sánchez HF (2006) The distribution and ecological preferences of Boophilus microplus (Acari:Ixodidae) in Mexico. Exp Appl Acarol 38:307–316

    Article  PubMed  Google Scholar 

  • FAO (2004) Acaricide Resistance: Diagnosis, Management and Prevention. Guidelines Resistance Management and Integrated Parasite Control in Ruminants, Animal Production and Health Division, Agriculture Department, Food and Agriculture Organization of the United Nations, Rome, 25–77

  • Figueiredo A, Agnolon IC, Lopes LG, Giglioti R, Chagas AC (2018) Comparative study of hatching estimation methods of Rhipicephalus (Boophilus) microplus eggs. Vet Parasitol 264:35–38

    Article  PubMed  Google Scholar 

  • Finney DJ (1962) Probit analysis, vol 78. Cambridge University Press, Cambridge, pp 388–390

    Google Scholar 

  • Fouche G, Sakong BM, Adenubi OT (2017) Investigation of the acaricidal activity of the acetone and ethanol extracts of 12 South African plants against the adult ticks of Rhipicephalus turanicus. Onderstepoort j Vet Res 84:1–7

    Article  CAS  Google Scholar 

  • Frame AD, Ríos-Olivares E, De Jesús L, Ortiz D, Pagán J, Méndez S (1998) Plants from Puerto Rico with anti-Mycobacterium tuberculosis properties. P R Health Sci J 17:243–252

    CAS  PubMed  Google Scholar 

  • Gallardo-Casas CA, Guevara-Balcázar G, Morales-Ramos E (2012) Ethnobotanic study of Randia aculeata (Rubiaceae) in Jamapa, Veracruz, Mexico, and its anti-snake venom effects on mouse tissue. J Venom Anim Toxins Incl Trop Dis 18:287–294

    Article  Google Scholar 

  • Ghosh S, Tiwari SS, Kumar B (2015) Identification of potential plant extracts for anti-tick activity against acaricide resistant cattle ticks, Rhipicephalus (Boophilus) microplus (Acari:Ixodidae). Exp Appl Acarol 66:59–171

    Article  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 23:150–156

    Article  PubMed  Google Scholar 

  • Khan S, Basra SMA, Afzal I, Nawaz M, Rehman HU (2017) Growth promoting potential of fresh and stored Moringa oleifera leaf extracts in improving seedling vigor, growth and productivity of wheat crop. Environ Sci Pollut Res 24:27601–27612

    Article  CAS  Google Scholar 

  • Khan A, Nasreen N, Niaz S et al (2019) Acaricidal efficacy of Calotropis procera (Asclepiadaceae) and Taraxacum officinale (Asteraceae) against Rhipicephalus microplus from Mardan, Pakistan. Exp Appl Acarol 78:595–608

    Article  CAS  PubMed  Google Scholar 

  • Kostyukovsky M, Gileadi C, Demchenko N, Shaaya E (2002) Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci 58:1101–1106

    Article  CAS  PubMed  Google Scholar 

  • Kovendan K, Murugan K, Naresh Kumar A, Vincent S, Hwang JS (2012) Bioefficacy of larvicdial and pupicidal properties of Carica papaya (Caricaceae) leaf extract and bacterial insecticide, spinosad, against chikungunya vector, Aedes aegypti (Diptera: Culicidae). Parasitol Res 110:669–678

    Article  PubMed  Google Scholar 

  • Lopez MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crops and Prod 31:284–288

    Article  CAS  Google Scholar 

  • Manzoor M, Ali H, Muhammad A, Alam I, Khalid SH, Idrees A, Arif M (2015) Potential of Moringa (Moringa oleifera: Moringaceae) as plant growth regulator and bio-pesticide against wheat aphids on wheat crop (Triticum aestivum; Poaceae). J Biopest 8:120–127

    Google Scholar 

  • Miraballes C, Riet-Correa F (2018) A review of the history of research and control of Rhipicephalus (Boophilus) microplus, babesiosis and anaplasmosis in Uruguay. Exp Appl Acarol 75:383–398

    Article  CAS  PubMed  Google Scholar 

  • Moreau TL, Isman MB (2012) Combining reduced-risk products, trap crops and yellow sticky traps for greenhouse whitefly (Trialeurodes vaporariorum) management on sweet peppers (Capsicum annum). Crop Prot 34:42–46

    Article  CAS  Google Scholar 

  • Muhammad SN (2012) Effects of plant extracts on the behaviour and physiology of the Odontotermes obesus (Ramb.) (Isoptera: Termitidae). Dissertation. University of Agriculture, Faisalabad, Pakistan

  • Niezen JH, Charleston WAG, Robertson HA, Shelton D, Waghorn GC, Green R (2002) The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and immunity to gastrointestinal nematodes. Vet Parasitol 105:229–245

    Article  CAS  PubMed  Google Scholar 

  • Nwankwo EN, Okonkwo NJ, Ogbonna CU, Akpom CJ, Egbuche CM, Ukonze BC (2015) Moringa oleifera and Annona muricataseed oil extracts as biopesticides against the second and fourth larval instar ofAedes aegypti L. (Diptera: Culicidae). J Biopest 8:56–61

    CAS  Google Scholar 

  • O’Callaghan FE, Neilson R, MacFarlane SA (2019) Dynamic biospeckle analysis, a new tool for the fast screening of plant nematicide selectivity. Plant Methods 15:1–13

    Article  CAS  Google Scholar 

  • Oliveira CFR, Luz LA, Paiva PMG, Coelho LCBB, Marangoni S, Macedo MLR (2011) Evaluation of seed coagulant Moringa oleifera lectin (cMoL) as a bioinsecticidal tool with potential for the control of insects. Process Biochem 46:498–504

    Article  CAS  Google Scholar 

  • Omoregie M, Omoregie A, Iloba B (2018) Insecticidal potential of Moringa oleifera (Lamarck) root on workers of Macrotermes bellicosus (Smeathman). EIJST 7:9–16

    Google Scholar 

  • Paiva PMG, Santana GMS, Souza IFAC, Albuquerque LP, Agra-Neto AC, Albuquerque AC, Luz LA, Napoleão TH, Coelho LCBB (2010) Effect of lectins from Opuntia ficus indica cladodes and Moringa oleifera seeds on survival of Nasutitermes corniger. Int Biodeter Biodegrad 65:982–989

    Article  CAS  Google Scholar 

  • Pandey A, Tripathi SM (2014) Concept of standardization, extraction and pre phytochemical screening strategies for herbal drug. J Pharmacogn Phytochem 2:115–119

    Google Scholar 

  • Pontual EV, Napoleão TH, Dias de Assis CR (2012) Effect of Moringa oleifera flower extract on larval trypsin and acetylcholinesterase activities in Aedes aegypti. Arch Insect Biochem Physiol 79:135–152

    Article  CAS  PubMed  Google Scholar 

  • Rashed KN, da Cruz MG, Vieira GPG, Magalhaes LG, Cunha WR (2013) Evaluation of schistosomicidal and leishmanicidal activities from Carica papaya (Linn.) stem and phytochemical composition. J Herbal Med 2:239–243

    Google Scholar 

  • Rawani A, Mallick HK, Ghosh A, Chandra G (2009) Larvicidal activities of three plants against filarial vector Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol Res 105:1411–1417

    Article  PubMed  Google Scholar 

  • Ribeiro VL, Vanzella C, Moysés S, Santos JC, Martins JR, Von Poser GL, Siqueira IR (2012) Effect of Calea serrata Less. n-hexane extract on acetylcholinesterase of larvae ticks and brain Wistar rats. Vet Parasitol 189:322–326

    Article  PubMed  Google Scholar 

  • Rosado-Aguilar JA, Arjona-Cambranes K, Torres-Acosta JFJ (2017) Plant products and secondary metabolites with acaricide activity against ticks. Vet Parasitol 238:66–76

    Article  CAS  PubMed  Google Scholar 

  • Roulston WJ, Schnitzerling HJ, Schuntner CA (1968) Acetylcholinesterase insensitivity in the Biarra strain of the cattle tick Boophilus microplus, as a cause of resistance to organophosphorus and carbamate acaricides. Aust J Biol Sci 21:759–768

    Article  CAS  PubMed  Google Scholar 

  • Sharma AK, Kumar R, Kumar S, Nagar G, Singh NK, Rawat SS, Dhakad M, Rawat A, Ray D, Ghosh S (2012) Deltamethrin and cypermethrin resistance status of Rhipicephalus (Boophilus) microplus collected from six agro-climatic regions of india. Vet Parasitol 188:337–345

    Article  CAS  PubMed  Google Scholar 

  • Sholapur HPN, Patil BM (2013) Pharmacognostic and phytochemical investigations on the bark of Moringa oleifera Lam. Indian J Nat Prod Resour 4:96–101

    Google Scholar 

  • Shyma KP, Gupta JP, Ghosh S, Patel K, Singh V (2014) Acaricidal effect of herbal extracts against cattle tick Rhipicephalus (Boophilus) microplus using in vitro studies. Parasitol Res 113:1–8

    Article  Google Scholar 

  • Singh NK, Miller RJ, Klafke GM, Goolsby JA, Thomas DB, de Leon AAP (2018) In-vitro efficacy of a botanical acaricide and its active ingredients against larvae of susceptible and acaricide-resistant strains of Rhipicephalus (Boophilus) microplus Canestrini (Acari: Ixodidae). Ticks Tick-Borne Dis 9:201–206

    Article  PubMed  Google Scholar 

  • Soto A, Castillo B, Delgado A, González A, Montenegro R (2001) Alkaloid screening of herbarium samples of Rubiaceae from Panama. Pharm Biol 39:161–169

    Article  Google Scholar 

  • Torres-Fajardo RA, Navarro-Alberto JA, Ventura-Cordero J (2019) Intake and selection of goats grazing heterogeneous vegetation: Effect of gastrointestinal nematodes and condensed tannins. Rangel Ecol Manag 72:946–953

    Article  Google Scholar 

  • Vij T, Prashar Y (2015) A review on medicina properties of Carica papaya Linn. Asian Pacific J Trop Dis 5:1–6

    Article  Google Scholar 

  • Walker AR, Bouattour Camicas J, Estrada-Peña L, Horak A, Latif IG, Pegram AA, Preston PM (2007) Ticks of domestic animals in africa: a guide to identifcation of species. Edinburgh Bioscience Reports, UK

    Google Scholar 

  • Yusha’u M, Onuorah F, Murtala Y, (2009) In vitro sensitivity pattern of some urinary tract isolates to Carica papaya extracts. Bayero J Pure Appl Sci 2:75–78

    Google Scholar 

  • Zaman MA, Iqbal Z, Abbas RZ, Khan MN, Muhammad G, Younus M, Ahmed S (2012) In vitro and in vivo acaricidal activity of an herbal extract. Vet Parasitol 186:431–436

    Article  PubMed  Google Scholar 

  • Zobayer N, Hasan R (2013) Effects of manually processed bio-pesticides on crop production and pest managements in Okra (Abelmoschus esculentus (L.) Moench). J Nat Sci Res 3:112–116

    Google Scholar 

Download references

Acknowledgements

We thank Cátedras-CONACyT project 1028 and project CONACYT-CB/2016-284813. JL Bravo-Ramos thanks CONACyT for scholarship 781463, Mexico. The authors would like to thank Daniel Zamudio Aguilar for generously contributing recollected tick strains to the current study, Dr. Francisco T. Barradas Piña for training in bioassays and Dr. D. Paniagua-Vega for granting the M. oleifera root powder.

Author information

Authors and Affiliations

  1. Unidad de Diagnóstico, Laboratorio de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Rancho ‘Torreón del Molino’, Universidad Veracruzana, CP 91710, Veracruz, Veracruz, Mexico

    J. L. Bravo-Ramos, A. Cruz-Romero & D. Romero-Salas

  2. Facultad de Medicina Veterinaria y Zootecnia, Laboratorio de Bioquímica, Universidad Veracruzana, CP 91710, Veracruz, Veracruz, Mexico

    A. Flores-Primo

  3. Facultad de Medicina, Departamento de Química Analítica, Universidad Autónoma de Nuevo León, Av. Fco. I. Madero y Dr. E. Aguirre Pequeño s/n, CP 64460, Monterrey, Nuevo León, Mexico

    D. Paniagua-Vega

  4. Catedras CONACYT-UANL, San nicolás de los garza, Mexico

    D. Paniagua-Vega

  5. Facultad de Bioanálisis, Universidad Veracruzana, CP 91700, Veracruz, Veracruz, Mexico

    M. G. Sánchez-Otero

Authors
  1. J. L. Bravo-Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Flores-Primo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Paniagua-Vega
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. G. Sánchez-Otero
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Cruz-Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. Romero-Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JLB-R wrote the manuscript. DR-S provided the biological material of Randia aculeata. DR-S, AF-P, DP-V, AC-R and MGS-O designed the project. JLBR, collected tick samples, identified tick species collected, and performed laboratory assays. MGSO, AFP performed extractions.

Corresponding author

Correspondence to D. Romero-Salas.

Ethics declarations

Conflict of interest

The authors declared that there are no conflicts of interest among them.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bravo-Ramos, J.L., Flores-Primo, A., Paniagua-Vega, D. et al. Acaricidal activity of the hexanic and hydroethanolic extracts of three medicinal plants against southern cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Exp Appl Acarol 85, 113–129 (2021). https://doi.org/10.1007/s10493-021-00654-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-021-00654-y

Keywords

Search

Navigation