Cytotoxic effects of Satureja montana L. essential oil on oocytes of engorged Rhipicephalus microplus female ticks (Acari: Ixodidae).
Satureja montana L.
cattle tick
essential oil
ovary morphology
tick control
Journal
Microscopy research and technique
ISSN: 1097-0029
Titre abrégé: Microsc Res Tech
Pays: United States
ID NLM: 9203012
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
revised:
16
11
2020
received:
21
07
2020
accepted:
21
12
2020
pubmed:
7
1
2021
medline:
19
8
2021
entrez:
6
1
2021
Statut:
ppublish
Résumé
In addition to pesticidal activity, the capacity of natural compounds to inhibit the reproduction of parasites emerge as an important alternative tick control method. In this context, Satureja spp. stand out due to their recognized pesticidal properties. Among parasites of veterinary importance, the cattle tick, Rhipicephalus microplus, is responsible for great economic losses in livestock and transmission of relevant pathogens. Thus, the aim of this study was to evaluate the effects of different concentrations of the essential oil of Satureja montana L. on the ovary morphology of R. microplus engorged females through histological and histochemical techniques. The most remarkable morphological changes found were: cytoplasmic vacuolation of germ cells, irregular and thicker chorion, irregular oocyte shape, ring-shaped nucleolus, decrease in protein and carbohydrate content in oocytes, in addition to cellular changes in the oviduct and pedicel. All morphological changes were assessed using a semiquantitative method already established in the literature. Ticks exposed to 5.0 μl/ml of essential oil showed the most significant changes when compared to control groups. Thus, the essential oil of S. montana L. damaged the reproductive system of R. microplus, which may impair ticks' offspring production and promote a long-term control of this species. HIGHLIGHTS: The essential oil of Satureja montana L. affects the ovary morphology of the cattle tick. The main morphological alterations found were cytoplasmic vacuolation, irregular and thicker chorion and irregular oocyte shape. These alterations may impair the development of eggs.
Substances chimiques
Oils, Volatile
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1375-1388Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 430327/2018-8
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Abbas, R. Z., Zaman, M. A., Colwell, D. D., Gilleard, J., & Iqbal, Z. (2014). Acaricide resistance in cattle ticks and approaches to its management: The state of play. Veterinary Parasitology, 203, 6-20. https://doi.org/10.1016/j.vetpar.2014.03.006
Adams, R. P. (2017). Identification of essential oil components by gas chromatography/mass spectrometry (4th ed., p. 804). Carol Streem: Allure.
Adenubi, O. T., Ahmed, A. S., Fasina, F. O., McGaw, L. J., Eloff, J. N., & Naidoo, V. (2018). Pesticidal plants as a possible alternative to synthetic acaricides in tick control: A systematic review and meta-analysis. Industrial Crops and Products, 123, 779-806. https://doi.org/10.1016/j.indcrop.2018.06.075
Araújo, L. X., Novato, T. P. L., Zeringota, V., Maturano, R., Melo, D., da Silva, B. C., … Monteiro, C. M. O. (2016). Synergism of thymol, carvacrol and eugenol in larvae of the cattle tick, Rhipicephalus microplus, and brown dog tick, Rhipicephalus sanguineus. Medical and Veterinary Entomology, 30, 377-382. https://doi.org/10.1111/mve.12181
Balashov, Y. S. (1983). Atlas of ixodid tick ultrastructure (p. 239). USA: Entomological Society of Amer.
Barbosa, C. S., Borges, L. M. F., Louly, C. C. B., Rocha, T. L., de Sabóia-Morais, S. M. T., Miguita, C. H., … Garcez, F. R. (2016). In vitro activity of 3β-O-tigloylmelianol from Guarea kunthiana A. Juss (Meliaceae) on oogenesis and ecdysis of the cattle tick Rhipicephalus (Boophilus) microplus (Canestrini) (Acari: Ixodidae). Experimental Parasitology, 164, 5-11. https://doi.org/10.1016/j.exppara.2016.01.015
Benelli, G., Pavela, R., Canale, A., Cianfaglione, K., Ciaschetti, G., Conti, F., … Maggi, F. (2017). Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: Synergistic and antagonistic effects. Parasitology International, 66, 166-171. https://doi.org/10.1016/j.parint.2017.01.012
Borges, L. M. F., de Sousa, L. A. D., & Barbosa, C. d. S. (2011). Perspectives for the use of plant extracts to control the cattle tick Rhipicephalus (Boophilus) microplus. Revista Brasileira de Parasitologia Veterinária, 20, 89-96. https://doi.org/10.1590/s1984-29612011000200001
Camargo-Mathias, M.I. (2018). Inside ticks: Morphophysiology, toxicology and therapeutic perspectives. Editora Unesp, São Paulo.
Cetin, H., Cilek, J. E., Oz, E., 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). Veterinary Parasitology, 170, 287-290. https://doi.org/10.1016/j.vetpar.2010.02.031
Dantas-Torres, F. (2008). The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): From taxonomy to control. Veterinary Parasitology, 152, 173-185. https://doi.org/10.1016/j.vetpar.2007.12.030
De Clercq, E. M., Vanwambeke, S. O., Sungirai, M., Adehan, S., Lokossou, R., & Madder, M. (2012). Geographic distribution of the invasive cattle tick Rhipicephalus microplus, a country-wide survey in Benin. Experimental and Applied Acarology, 58(4), 441-452. https://doi.org/10.1007/s10493-012-9587-0
Denardi, S. E., Bechara, G. H., Oliveira, P. R., & Camargo-Mathias, M. I. (2011). Inhibitory action of neem aqueous extract (Azadirachta indica A. Juss) on the Vitellogenesis of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) ticks. Microscopy Research and Technique, 74, 889-899. https://doi.org/10.1002/jemt.20973
Drummond, R. O., Ernst, S. E., Trevino, J. L., Gladney, W. J., & Graham, O. H. (1973). Tests of acaricides for control of Boophilus annulatus and B. microplus. Journal of Economic Entomology, 69, 37-40. https://doi.org/10.1093/jee/69.1.37
Dunkic̈, V., Kremer, D., Dragojevic̈ Müller, I., Stabentheiner, E., Kuzmic̈, S., Jurišic̈ Grubešic̈, R., … Bezic̈, N. (2012). Chemotaxonomic and micromorphological traits of Satureja montana L. and S. subspicata Vis. (Lamiaceae). Chemistry & Biodiversity, 9, 2825-2842. https://doi.org/10.1002/cbdv.201100376
Grisi, L., Leite, R. C., Martins, J. R. S., Barros, A. T. M., Andreotti, R., Cançando, P. H. D., León, A. A. P., Pereira, J. B., Vilela, H. S. (2014). Reassessment of the potential economic impact of cattle parasites in Brazil. Revista Brasileira de Parasitologia Veterinária, 23, 150-156. https://doi.org/10.1590/S1984-29612014042
Guerrero, F. D., Lovis, L., & Martins, J. R. (2012). Acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus. Revista Brasileira de Parasitologia Veterinária, 21, 1-6. https://doi.org/10.1590/s1984-29612012000100002
Heydarzade, A., & Moravvej, G. (2012). Contact toxicity and persistence of essential oils from Foeniculum vulgare, Teucrium polium and Satureja hortensis against Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) adults. Turkiye Entomoloji Dergisi, 36, 507-518. https://doi.org/10.16970/ted.56583
Higa, L. O. S., Garcia, M. V., Barros, J. C., Koller, W. W., & Andreotti, R. (2015). Acaricide resistance status of the Rhipicephalus microplus in Brazil: A literature overview. Medicinal Chemistry, 5, 326-333. https://doi.org/10.4172/2161-0444.1000281
Hinton, H. E. (1981). Biology of insect eggs. Oxford: Pergamon Press.
Jonsson, N. N. (2006). The productivity effects of cattle tick (Boophilus microplus) infestation on cattle, with particular reference to Bos indicus cattle and their crosses. Veterinary Parasitology, 137, 1-10. https://doi.org/10.1016/j.vetpar.2006.01.010
Junqueira, L. C. U., & Junqueira, L. M. M. S. (1983). Técnicas básicas de citologia e histologia (p. 123). São Paulo: Santos.
Konig, I. F. M., Gonçalves, R. R. P., Oliveira, M. V. S., Silva, C. M., Thomasi, S. S., Peconick, A. P., & Remedio, R. N. (2019). Sublethal concentrations of acetylcarvacrol strongly impact oocyte development of engorged female cattle ticks Rhipicephalus microplus (Canestrini, 1888) (Acari: Ixodidae). Ticks and Tick-Borne Diseases, 10, 766-774. https://doi.org/10.1016/j.ttbdis.2019.03.010
Konig, I. F. M., Oliveira, M. V. S., Gonçalves, R. R. P., Peconick, A. P., Thomasi, S. S., Anholeto, L. A., … Remedio, R. N. (2020). Low concentrations of acetylcarvacrol induce drastic morphological damages in ovaries of surviving Rhipicephalus sanguineus sensu lato ticks (Acari: Ixodidae). Micron, 129, 102780. https://doi.org/10.1016/j.micron.2019.102780
Lima de Souza, J. R., de Oliveira, P. R., Anholeto, L. A., Arnosti, A., Daemon, E., Remedio, R. N., & Camargo-Mathias, M. I. (2019). Effects of carvacrol on oocyte development in semi-engorged Rhipicephalus sanguineus sensu lato females ticks (Acari: Ixodidae). Micron, v, 116, 66-72.
Maedeh, M., Hamzeh, I., Hossein, D., Majid, A., & Reza, R. K. (2011). Bioactivity of essential oil from Satureja hortensis (Laminaceae) against three stored-product insect species. African. Journal of Biotechnology, 10, 6620-6627. https://doi.org/10.5897/AJB11.469
Matos, R., Daemon, E., Camargo-Mathias, M. I., Furquim, K. C. S., Sampieri, B. R., Remédio, R. N., … Novato, T. P. L. (2014). Histopathological study of ovaries of Rhipicephalus sanguineus (Acari: Ixodidae) exposed to different thymol concentrations. Parasitology Research, 113, 4555-4565. https://doi.org/10.1007/s00436-014-4145-9
Michaelakis, A., Theotokatos, S. A., Koliopoulos, G., & Chorianopoulos, N. G. (2007). Essential oils of Satureja species: Insecticidal effect on Culex pipiens larvae (Diptera: Culicidae). Molecules, 12, 2567-2578. https://doi.org/10.3390/12122567
Novato, T. L. P., Araújo, L. X., Monteiro, C. M. O., Maturano, R., Senra, T. O. S., Silva-Matos, R., … Daemon, E. (2015). Evaluation of the combined effect of thymol, carvacrol and (E)-cinnamaldehyde on Amblyomma sculptum (Acari: Ixodidae) and Dermacentor nitens (Acari: Ixodidae) larvae. Veterinary Parasitology, 212, 331-335. https://doi.org/10.1016/j.vetpar.2015.08.021
Novato, T. L. P., Marchesini, P., Muniz, N., Prata, M. C. A., Furlong, J., Viliela, F. M. P., … Monterio, C. (2019). Evaluation of synergism and development of a formulation with thymol, carvacrol and eugenol for Rhipicephalus microplus control. Experimental Parasitology, 207, 107774. https://doi.org/10.1016/j.exppara.2019.107774
Oliveira, P., Anholeto, L., Ferreira Rodrigues, R., Arnosti, A., Bechara, G., de Carvalho Castro, K., & Camargo-Mathias, M. (2019). Cytotoxic effects of extract of Acmella oleracea in the ovaries and midgut of Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) female ticks. Journal of Microscopy and Ultrastructure, 7, 28-43. https://doi.org/10.4103/jmau.jmau_16_18
Oliveira, P. R., Bechara, G. H., & Camargo-Mathias, M. I. (2008). Evaluation of cytotoxic effects of fipronil on ovaries of semi-engorged Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick female. Food and Chemical Toxicology, 46, 2459-2465. https://doi.org/10.1016/j.fct.2008.03.034
Oliveira, P. R., de Carvalho Castro, K. N., Anholeto, L. A., & Camargo Mathias, M. I. (2016). Cytotoxic effects of extract of Acmella oleraceae (Jambú) in Rhipicephalus microplus females ticks. Microscopy Research and Technique, 79, 744-753. https://doi.org/10.1002/jemt.22693
Oliveira, T. L. C., de Araújo Soares, R., Ramos, E. M., das Graças Cardoso, M., Alves, E., & Piccoli, R. H. (2011). Antimicrobial activity of Satureja montana L. essential oil against Clostridium perfringens type a inoculated in mortadella-type sausages formulated with different levels of sodium nitrite. International Journal of Food Microbiology, 144, 546-555. https://doi.org/10.1016/j.ijfoodmicro.2010.11.022
Oliveira, T. L. C., Malfitano de Carvalho, S., de Araújo Soares, R., Andrade, M. A., Cardoso, M. d. G., Ramos, E. M., & Piccoli, R. H. (2012). Antioxidant effects of Satureja montana L. essential oil on TBARS and color of mortadella-type sausages formulated with different levels of sodium nitrite. LWT - Food Science and Technology, 45, 204-212. https://doi.org/10.1016/j.lwt.2011.09.006
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. Research in Veterinary Science, 109, 1-9. https://doi.org/10.1016/j.rvsc.2016.09.001
Pearse, A. (1985). Histochemistry theoretical and applied. Edinburgh: Churchill Livingstone.
Pereira-Junior, A. M., Camargo-Mathias, M. I., Daemon, E., Peconick, A. P., Lima-Souza, J. R., Oliveira, P. R., … Remedio, R. N. (2019). Efficacy of carvacrol on Rhipicephalus (Boophilus) microplus engorged female ticks (Canestrini, 1887) (Acari: Ixodidae): Effects on mortality and reproduction. Natural Product Research, 0, 1-4. https://doi.org/10.1080/14786419.2019.1569657
Piccaglia, R., Marotti, M., & Galletti, G. C. (1991). Characterization of essential oil from a Satureja montana L. Chemotype grown in northern Italy. Journal of Essential Oil Research, 3, 147-152. https://doi.org/10.1080/10412905.1991.9700494
Remedio, R. N., Nunes, P. H., Anholeto, L. A., Oliveira, P. R., & Camargo-Mathias, M. I. (2014). Morphological effects of neem (Azadirachta indica a. Juss) seed oil with known azadirachtin concentrations on the oocytes of semi-engorged Rhipicephalus sanguineus ticks (Acari: Ixodidae). Parasitology Research, 114, 431-444. https://doi.org/10.1007/s00436-014-4200-6
Rodriguez-Vivas, R. I., Jonsson, N. N., & Bhushan, C. (2017). Strategies for the control of Rhipicephalus microplus ticks in a world of conventional acaricide and macrocyclic lactone resistance. Parasitology Research, 117(1), 3-29. https://doi.org/10.1007/s00436-017-5677-6
Rodriguez-Vivas, R. I., Trees, A. J., Rosado-Aguilar, J. A., Villegas-Perez, S. L., & Hodgkinson, J. E. (2011). Evolution of acaricide resistance: Phenotypic and genotypic changes in field populations of Rhipicephalus (Boophilus) microplus in response to pyrethroid selection pressure. International Journal for Parasitology, 41(8), 895-903. https://doi.org/10.1016/j.ijpara.2011.03.012
Roma, G. C., Bechara, G. H., & Camargo Mathias, M. I. (2010). Permethrin-induced ultrastructural changes in oocytes of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females. Ticks and Tick-Borne Diseases, 1, 113-123. https://doi.org/10.1016/j.ttbdis.2010.05.004
Rosado-Aguilar, J. A., Aguilar-Caballero, A., Rodriguez-Vivas, R. I., Borges-Argaez, R., Garcia-Vazquez, Z., & Mendez-Gonzalez, M. (2010). Acaricidal activity of extracts from Petiveria alliacea (Phytolaccaceae) against the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Veterinary Parasitology, 168, 299-303. https://doi.org/10.1016/j.vetpar.2009.11.022
Saito, K. C., Bechara, G. H., Nunes, É. T., Oliveira, P. R., Denardi, S. E., & Camargo-Mathias, M. I. (2005). Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Veterinary Parasitology, 129, 299-311. https://doi.org/10.1016/j.vetpar.2004.09.020
Sampieri, B. R., Arnosti, A., Nunes, P. H., Furquim, K. C. S., Chierice, G. O., & Mathias, M. I. C. (2012). Ultrastructural changes in the ovary cells of engorged Rhipicephalus sanguineus female ticks treated with esters of ricinoleic acid from castor oil (Ricinus communis). Microscopy Research and Technique, 75(5), 683-690.
Scheer, U., & Hock, R. (1999). Structure and function of the nucleolus. Current Opinion in Cell Biology, 11, 385-390. https://doi.org/10.1016/S0955-0674(99)80054-4
Serrano, C., Matos, O., Teixeira, B., Ramos, C., Neng, N., Nogueira, J., … Marques, A. (2011). Antioxidant and antimicrobial activity of Satureja montana L. extracts. Journal of the Science of Food and Agriculture, 91, 1554-1560. https://doi.org/10.1002/jsfa.4347
Sharma, A. K., Kumar, S., Tiwari, S. S., Srivastava, S., Kumar, R., Ray, D. D., … Ghosh, S. (2012). Comparative acaricidal properties of different solvents and surfactants on Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Indian Journal of Animal Sciences, 82, 154-158.
Sonenshine, D. E., & Roe, R. M. (2014). Biology of ticks. New York: Oxford University Press.
Stoilova, I., Bail, S., Buchbauer, G., Krastanov, A., Stoyanova, A., Schmidt, E., & Jirovetzb, L. (2008). Chemical composition, olfactory evaluation and antioxidant effects of the essential oil of Satureja montana L. Natural Product Communications, 1(4), 9-12.
Šućur, J., Popović, A., Petrović, M., Anačkov, G., Bursić, V., Kiprovski, B., & Prvulović, D. (2015). Allelopathic effects and insecticidal activity of aqueous extracts of Satureja montana L. Journal of the Serbian Chemical Society, 80, 475-484. https://doi.org/10.2298/JSC020714106S
Taban, A., Saharkhiz, M. J., & Hooshmandi, M. (2017). Insecticidal and repellent activity of three Satureja species against adult red flour beetles, Tribolium castaneum (Coleoptera: Tenebrionidae). Acta Ecologica Sinica, 37, 201-206. https://doi.org/10.1016/j.chnaes.2017.01.001
Tak, J. H., & Isman, M. B. (2017). Acaricidal and repellent activity of plant essential oil-derived terpenes and the effect of binary mixtures against Tetranychus urticae Koch (Acari: Tetranychidae). Industrial Crops and Products, 108, 786-792. https://doi.org/10.1016/j.indcrop.2017.08.003
Tozlu, E., Cakir, A., Kordali, S., Tozlu, G., Ozer, H., & Aytas Akcin, T. (2011). Chemical compositions and insecticidal effects of essential oils isolated from Achillea gypsicola, Satureja hortensis, Origanum acutidens and Hypericum scabrum against broadbean weevil (Bruchus dentipes). Scientia Horticulturae, 130, 9-17. https://doi.org/10.1016/j.scienta.2011.06.019
Troughton, D. R., & Levin, M. L. (2007). Life Cycles of Seven Ixodid Tick Species (Acari: Ixodidae) Under Standardized Laboratory Conditions. Journal of Medical Entomology, 44, 732-740. https://doi.org/10.1093/jmedent/44.5.732
Tsaboula, A., Papadakis, E. N., Vryzas, Z., Kotopoulou, A., Kintzikoglou, K., & Papadopoulou-Mourkidou, E. (2016). Environmental and human risk hierarchy of pesticides: A prioritization method, based on monitoring, hazard assessment and environmental fate. Environment International, 91, 78-93. https://doi.org/10.1016/j.envint.2016.02.008
Van den Dool, H., & Kratz, P. D. (1963). A generalization of the retention index system including linear temperature programmed gas-liquid parti-tion chromatography. Journal of Chromatography A, 11, 463-471.
Vendramini, M. C. R., Mathias, M. I. C., De Faria, A. U., Furquim, K. C. S., De Souza, L. P., Bechara, G. H., & Roma, G. C. (2012). Action of andiroba oil (Carapa guianensis) on Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females: Morphophysiological evaluation of reproductive system. Microscopy Research and Technique, 75, 1745-1754. https://doi.org/10.1002/jemt.22126
Yazdani, E., Sendi, J. J., Khosravi, R., Hajizadeh, J., & Ghadamyari, M. (2013). Effect of Satureja hortensis L. essential oil on feeding efficiency and biochemical properties of Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). Archives of Phytopathology and Plant Protection, 46, 328-339. https://doi.org/10.1080/03235408.2012.740980