Skip to main content
Log in

Study on In Vitro Acaricidal Proprieties of Pinus sylvestris Against Two Ectoparasites of Veterinary Importance Dermanyssus gallinae and Hyalomma scupense

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

The present study deals with the toxicity of Pinus sylvestris essential oil against red poultry mites Dermanyssus gallinae and Hyalomma scupense cattle ticks in laboratory condition. Individual essential oil components identified using a gas chromatograph/mass spectrometer, namely α-pinene (44.92%), β-pinene (17.51%), δ-3 carene (16.18%) and D-Limonene (9.21%) were tested as well as. For this purpose, different doses (0.31; 0.62; 1.25 and 2.5 mg/mL) of essential oil and four monoterpenes using mites contact and spraying in vitro bioassays were carried out. Amitraz and thymol (positive controls), and ethanol and distilled water (negative controls) were also tested each with three replications. Tick larvicidal and ovicidal assays were done testing 0.5; 1; 2 and 4 mg/mL of the P. sylvestris essential oil and its main components. The experiment results from mites revealed that the spraying application method was more effective than the contact bioassay for acaricidal property when P. sylvestris essential oil was toxic to D. gallinae with LC50 values of 0.68 mg/mL. Larvicidal and ovicidal assays revealed the promising activity of the essential oil against tick larvae and eggs. Among all the tested compounds, D-Limonene appears as the most toxic essential oil constituent for both ticks and mites, showing LC50 values lower than the whole essential oil. δ-3-carene was slightly toxic, with LC50 values higher than the whole essential oil, whereas α-pinene and β-pinene showed weak acaricidal activity even at high concentration. On the other hand, P. sylvestris essential oil and its principal components were tested for acetyl-cholinesterase inhibitory activity using Ellman’s colorimetric method and compared to a reference galantamine. Interestingly the monoterpene D-Limonene was found the most active AchE inhibitor (IC50 = 27.22 µg/mL), almost comparable to that of positive control. Overall, our research pointed out the importance of the traditional use of P. sylvestris as an ecofriendly alternative against ectoparasites of veterinary importance; D. gallinae and H. scupense. In vivo trials should also be conducted to assure the safe use of natural plants.

Graphical Abstract

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article.

References

  1. Muhammad, A., Bashir, R., Mahmood, M., Afzal, M.S., Simsek, S., Awan, U.A., Khan, M.R., Ahmed, H., Cao, J.: Epidemiology of ectoparasites (Ticks, Lice, and Mites) in the livestock of Pakistan: a review. Front. Vet. Sci. 8, 780738 (2021). https://doi.org/10.3389/fvets.2021.780738

    Article  Google Scholar 

  2. Petersen, I., Johannhörster, K., Pagot, E., Escribano, D., Zschiesche, E., Temple, D., Thomas, E.: Assessment of fluralaner as a treatment in controlling Dermanyssus gallinae infestation on commercial layer farms and the potential for resulting benefits of improved bird welfare and productivity. Parasit. Vector 14, 181 (2021). https://doi.org/10.1186/s13071-021-04685-7

    Article  Google Scholar 

  3. Gharbi, M., Hayouni, M.E., Sassi, L., Dridi, W., Darghouth, M.A.: Hyalomma scupense (Acari, Ixodidae) in northeast Tunisia: seasonal population dynamics of nymphs and adults on field cattle. Parasite 20, 12 (2013). https://doi.org/10.1051/parasite/2013012

    Article  Google Scholar 

  4. Dziedziński, M., Kobus-Cisowska, J., Stachowiak, B.: Pinus species as prospective reserves of bioactive compounds with potential use in functional food—current state of knowledge. Plants 10, 1306 (2021). https://doi.org/10.3390/plants10071306

    Article  Google Scholar 

  5. Fekih, N., Allali, H., Merghache, S., Chaïb, F., Merghache, D., El Amine, M., Djabou, N., Muselli, A., Tabti, B., Costa, J.: Chemical composition and antibacterial activity of Pinus halepensis Miller growing in West Northern of Algeria. Asian Pac. J. Trop. Dis. 4, 97–103 (2014). https://doi.org/10.1016/S2222-1808(14)60323-6

    Article  Google Scholar 

  6. Teranishi, R., Buttery, R.G., Sugisawa, H. (eds.): Bioactive Volatile Compounds from Plants. American Chemical Society, Washington (1993)

    Google Scholar 

  7. Adjaoud, A., Laouer, H., Braca, A., Cioni, P., Moussi, K., Berboucha-Rahmani, M., Abbaci, H., Falconieri, D.: Chemical composition, antioxidant and insecticidal activities of a new essential oil chemotype of Pinus nigra ssp. mauritanica (Pinaceae), Northern Algeria. Plant Biosyst. 156, 358–369 (2022). https://doi.org/10.1080/11263504.2020.1857871

    Article  Google Scholar 

  8. Piccialli, I., Tedeschi, V., Caputo, L., Amato, G., De Martino, L., De Feo, V., Secondo, A., Pannaccione, A.: The antioxidant activity of limonene counteracts neurotoxicity triggered byAβ1-42 oligomers in primary cortical neurons. Antioxidants 10, 937 (2021). https://doi.org/10.3390/antiox10060937

    Article  Google Scholar 

  9. Mitić, Z.S., Jovanović, B., Jovanović, S.Č, Mihajilov-Krstev, T., Stojanović-Radić, Z.Z., Cvetković, V.J., Mitrović, T.L.J., Marin, P.D., Zlatković, B.K., Stojanović, G.S.: Comparative study of the essential oils of four Pinus species: chemical composition, antimicrobial and insect larvicidal activity. Ind. Crops Prod. 111, 55–62 (2018). https://doi.org/10.1016/j.indcrop.2017.10.004

    Article  Google Scholar 

  10. Ulukanli, Z., Karabörklü, S., Bozok, F., Ates, B., Erdogan, S., Cenet, M., Karaaslan, M.G.: Chemical composition, antimicrobial, insecticidal, phytotoxic and antioxidant activities of Mediterranean Pinus brutia and Pinus pinea resin essential oils. Chin. J. Nat. Med. 12, 901–910 (2014). https://doi.org/10.1016/S1875-5364(14)60133-3

    Article  Google Scholar 

  11. Macchioni, F., Cioni, P.L., Flamini, G., Morelli, I., Perrucci, S., Franceschi, A., Macchioni, G., Ceccarini, L.: Acaricidal activity of pine essential oils and their main components against Tyrophagus putrescentiae, a stored food mite. J. Agric. Food Chem. 50, 4586–4588 (2002). https://doi.org/10.1021/jf020270w

    Article  Google Scholar 

  12. Anderson, J.A., Coats, J.R.: Acetylcholinesterase inhibition by nootkatone and carvacrol in arthropods. Pestic. Biochem. Physiol. 102, 124–128 (2012). https://doi.org/10.1016/j.pestbp.2011.12.002

    Article  Google Scholar 

  13. Arafa, W.M., Aboelhadid, S.M., Moawad, A., Shokeir, K.M., Ahmed, O.: Toxicity, repellency and anti-cholinesterase activities of thymol-eucalyptus combinations against phenotypically resistant Rhipicephalus annulatus ticks. Exp. Appl. Acarol. 81, 265–277 (2020). https://doi.org/10.1007/s10493-020-00506-1

    Article  Google Scholar 

  14. Salleh, W.M.N.H.W., Khamis, S.: Chemical composition and anticholinesterase inhibitory activity of Pavetta graciliflora Wall. ex Ridl. essential oil. Z. Naturforsch. C 75, 467–471 (2020). https://doi.org/10.1515/znc-2020-0075

    Article  Google Scholar 

  15. Enan, E.: Insecticidal activity of essential oils: octopaminergic sites of action. Comp. Biochem. Physiol. Part-C: Toxicol. Pharmacol. 130, 325–337 (2001). https://doi.org/10.1016/S1532-0456(01)00255-1

    Article  Google Scholar 

  16. Jankowska, M., Rogalska, J., Wyszkowska, J., Stankiewicz, M.: Molecular targets for components of essential oils in the insect nervous system—a review. Molecules 23, 34 (2017). https://doi.org/10.3390/molecules23010034

    Article  Google Scholar 

  17. Blenau, W., Rademacher, E., Baumann, A.: Plant essential oils and formamidines as insecticides/acaricides: what are the molecular targets? Apidologie 43, 334–347 (2012). https://doi.org/10.1007/s13592-011-0108-7

    Article  Google Scholar 

  18. Priestley, C.M., Williamson, E.M., Wafford, K.A., Sattelle, D.B.: Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABA A receptors and a homo-oligomeric GABA receptor from Drosophila melanogaster: thymol enhances ionotropic GABA receptor activity. Br. J. Pharmacol. 140, 1363–1372 (2003). https://doi.org/10.1038/sj.bjp.0705542

    Article  Google Scholar 

  19. Adams, J.: The precautionary principle. Econ. Aff. 16, 6–10 (1995). https://doi.org/10.1111/j.1468-0270.1995.tb00504.x

    Article  Google Scholar 

  20. Kim, S.-I., Yi, J.-H., Tak, J., Ahn, Y.-J.: Acaricidal activity of plant essential oils against Dermanyssus gallinae (Acari: Dermanyssidae). Vet. Parasitol. 120, 297–304 (2004). https://doi.org/10.1016/j.vetpar.2003.12.016

    Article  Google Scholar 

  21. Baran, A.I., Jahanghiri, F., Hajipour, N., Sparagano, O.A.E., Norouzi, R., Moharramnejad, S.: In vitro acaricidal activity of essential oil and alcoholic extract of Trachyspermum ammi against Dermanyssus gallinae. Vet. Parasitol. 278, 109030 (2020). https://doi.org/10.1016/j.vetpar.2020.109030

    Article  Google Scholar 

  22. George, D.R., Smith, T.J., Shiel, R.S., Sparagano, O.A.E., Guy, J.H.: Mode of action and variability in efficacy of plant essential oils showing toxicity against the poultry red mite, Dermanyssus gallinae. Vet. Parasitol. 161, 276–282 (2009). https://doi.org/10.1016/j.vetpar.2009.01.010

    Article  Google Scholar 

  23. Stone, B.F., Haydock, K.P.: A method for measuring the acaricide-susceptibility of the cattle tick Boophilus microplus (Can.). Bull. Entomol. Res. 53, 563–578 (1962). https://doi.org/10.1017/S000748530004832X

    Article  Google Scholar 

  24. Ellman, G.L., Courtney, K.D., Andres, V., Featherstone, R.M.: A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88–95 (1961). https://doi.org/10.1016/0006-2952(61)90145-9

    Article  Google Scholar 

  25. Bonesi, M., Menichini, F., Tundis, R., Loizzo, M.R., Conforti, F., Passalacqua, N.G., Statti, G.A., Menichini, F.: Acetylcholinesterase and butyrylcholinesterase inhibitory activity of Pinus species essential oils and their constituents. J. Enzym. Inhib. Med. Chem. 25, 622–628 (2010). https://doi.org/10.3109/14756360903389856

    Article  Google Scholar 

  26. Roussis, V., Papadogianni, K., Vagias, C., Harvala, C., Petrakis, P.V., Ortiz, A.: Volatile constituents of three Pinus species grown in Greece. J. Essent. Oil Res. 13, 118–121 (2001). https://doi.org/10.1080/10412905.2001.9699632

    Article  Google Scholar 

  27. Hmamouchi, M., Hamamouchi, J., Zouhdi, M., Bessiere, J.M.: Chemical and antimicrobial properties of essential oils of five Moroccan Pinaceae. J. Essent. Oil Res. 13, 298–302 (2001). https://doi.org/10.1080/10412905.2001.9699699

    Article  Google Scholar 

  28. Dob, T., Berramdane, T., Chelgoum, C.: Chemical composition of essential oil of Pinus halepensis Miller growing in Algeria. C. R. Chim. 8, 1939–1945 (2005). https://doi.org/10.1016/j.crci.2005.05.007

    Article  Google Scholar 

  29. Ameur, E., Sarra, M.E., Mariem, K., Nabil, A., Lynen, F., Larbi, K.M.: Chemical composition of five Tunisian Pinus Species’ essential oils and effect of their blends on Otitis infection. Ind. Crops Prod. 180, 114688 (2022). https://doi.org/10.1016/j.indcrop.2022.114688

    Article  Google Scholar 

  30. López, M.D., Contreras, J., Pascual-Villalobos, M.J.: Selection for tolerance to volatile monoterpenoids in Sitophilus oryzae (L.), Rhyzopertha dominica (F.) and Cryptolestes pusillus (Schönherr). J. Stored Prod. Res. 46, 52–58 (2010). https://doi.org/10.1016/j.jspr.2009.09.003

    Article  Google Scholar 

  31. Langsi, J.D., Nukenine, E.N., Oumarou, K.M., Moktar, H., Fokunang, C.N., Mbata, G.N.: Evaluation of the insecticidal activities of α-Pinene and 3-carene on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Insects 11, 540 (2020). https://doi.org/10.3390/insects11080540

    Article  Google Scholar 

  32. da Silva, A.C.R., Lopes, P.M., de Azevedo, M.M.B., Costa, D.C.M., Alviano, C.S., Alviano, D.S.: Biological activities of a-Pinene and β-Pinene enantiomers. Molecules 17, 6305–6316 (2012). https://doi.org/10.3390/molecules17066305

    Article  Google Scholar 

  33. Alimi, D., Hajri, A., Jallouli, S., Sebai, H.: Phytochemistry, anti-tick, repellency, and anti-cholinesterase activities of Cupressus sempervirens L. and Mentha pulegium L. combinations against Hyalomma scupense (Acari: Ixodidae). Vet. Parasitol. 303, 109665 (2022). https://doi.org/10.1016/j.vetpar.2022.109665

    Article  Google Scholar 

  34. George, D.R., Sparagano, O.A.E., Port, G., Okello, E., Shiel, R.S., Guy, J.H.: Environmental interactions with the toxicity of plant essential oils to the poultry red mite Dermanyssus gallinae. Med. Vet. Entomol. 24, 1–8 (2010). https://doi.org/10.1111/j.1365-2915.2009.00855.x

    Article  Google Scholar 

  35. Kim, H.K., Lee, S.J., Hwang, B.-Y., Yoon, J.U., Kim, G.-H.: Acaricidal and repellent effects of Cnidium officinale-derived material against Dermanyssus gallinae (Acari: Dermanyssidae). Exp. Appl. Acarol. 74, 403–414 (2018). https://doi.org/10.1007/s10493-018-0249-8

    Article  Google Scholar 

  36. Dohi, S., Terasaki, M., Makino, M.: Acetylcholinesterase inhibitory activity and chemical composition of commercial essential oils. J. Agric. Food Chem. 57, 4313–4318 (2009). https://doi.org/10.1021/jf804013j

    Article  Google Scholar 

Download references

Acknowledgements

Special thanks go to Mr. Marouane Hafsi for allowing us to access and collect mites. The Authors, also, thank Mr. Ali Maiz, the farm owner, for allowing us to access and collect ticks. We appreciate everyone who took part in this process.

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

Authors

Contributions

Material preparation, data collection and analysis were performed by DA. All the manuscript was written by DA. SJ and AH contributed to the study conception, visualization and design. HS supervised and approved the final manuscript.

Corresponding author

Correspondence to Dhouha Alimi.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alimi, D., Hajri, A., Jallouli, S. et al. Study on In Vitro Acaricidal Proprieties of Pinus sylvestris Against Two Ectoparasites of Veterinary Importance Dermanyssus gallinae and Hyalomma scupense. Waste Biomass Valor 15, 337–347 (2024). https://doi.org/10.1007/s12649-023-02167-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-023-02167-8

Keywords

Navigation