Abstract
Haemaphysalis longicornis is one of the most prevalent tick species across eastern Asia, Australia, and New Zealand, and has been implicated as a vector of several pathogenic agents. This study evaluated the in vitro acaricidal efficacy of Cymbopogon citratus (lemongrass) essential oil on unfed H. longicornis using the adult and nymph immersion test, and the larval packet test. Six concentrations with three replications each of 10, 20, 30, 40, 50 and 60 mg/mL (adults and nymphs) were used, and 2.5, 5, 10, 20, 40 and 80 mg/mL (larvae), with control group (50% ethanol). The adult and nymph mortality rates were 98 and 100% at 50 mg/mL, and 95 and 100% at 60 mg/mL, respectively, whereas the larval mortality rate was 94 and 96% at 40 and 80 mg/mL, respectively. Mortality of adult, nymph and larva increased significantly in a dose-dependent manner. The LC50 for adult, nymph, and larva, were 29.21 (95% confidence interval 25.90–32.58), 28.18 (23.78–32.25), and 28.06 (25.57–30.90) mg/mL, respectively. Scanning electron microscopy and light microscopy revealed a disjointed sensilla base from the sockets, cuticular cracks, blocked aeropyles, and shrinking of the midgut. These results showed that C. citratus essential oil could be a good eco-friendly alternative control strategy against ectoparasites like ticks due to its high acaricidal efficacy.
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References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267
Aljedani DM (2017) Effects of abamectin and deltamethrin to the foragers honeybee workers of Apis mellifera jemenatica (Hymenoptera: Apidae) under laboratory conditions. Saudi J Biol Sci 24:1007–1015. https://doi.org/10.1016/j.sjbs.2016.12.007
Burgess IF (2009) The mode of action of dimeticone 4% lotion against head lice, Pediculus capitis. BMC Pharmacol 9:3. https://doi.org/10.1186/1471-2210-9-3
Cabezas-Cruz A, Valdés JJ (2014) Are ticks venomous animals? Front Zool 11:47. https://doi.org/10.1186/1742-9994-11-47
Catae AF, Roat TC, De Oliveira RA, Nocelli RCF, Malaspina O (2014) Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of africanized Apis mellifera (Hymenoptera: Apidae). Microsc Res Tech 77:274–281. https://doi.org/10.1002/jemt.22339
Chagas A, de Barros LD, Cotinguiba F, Furlan M, Giglioti R, de Sena Oliveira MC, Bizzo HR (2012) In vitro efficacy of plant extracts and synthesized substances on Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitol Res 110:295–303. https://doi.org/10.1007/s00436-011-2488-z
Chagas A, Domingues L, Fantatto RR, Giglioti R, Oliveira M, 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(1–2):277–284. https://doi.org/10.1016/j.vetpar.2014.06.030
Chakrabarti P, Rana S, Bandopadhyay S, Naik DG, Sarkar S, Basu P (2015) Field populations of native Indian honey bees from pesticide intensive agricultural landscape show signs of impaired olfaction. Sci Rep 5:12504. https://doi.org/10.1038/srep12504
Chen Z, Liu Q, Liu JQ, Xu BL, Lv S, Xia S, Zhou XN (2014) Tick-borne pathogens and associated co-infections in ticks collected from domestic animals in central China. Parasit Vectors 7:237. https://doi.org/10.1186/1756-3305-7-237
da Silva Cruz A, da Silva-Zacarin EC, Bueno OC, Malaspina O (2010) Morphological alterations induced by boric acid and fipronil in the midgut of worker honeybee (Apis mellifera L.) larvae: morphological alterations in the midgut of A. mellifera. Cell Biol Toxicol 26:165–176. https://doi.org/10.1007/s10565-009-9126-x
Dantas-Torres F (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors 3:26. https://doi.org/10.1186/1756-3305-3-26
De Meneghi D, Stachurski F, Adakal H (2016) Experiences in tick control by acaricide in the traditional cattle sector in Zambia and Burkina Faso: possible environmental and public health implications. Front Public Health 4:239. https://doi.org/10.3389/fpubh.2016.00239
de Monteiro CM, Maturano R, Daemon E, Catunda-Junior FEA, Calmon F, de Souza ST, Faza A, de Carvalho MG (2012) Acaricidal activity of eugenol on Rhipicephalus microplus (Acari: Ixodidae) and Dermacentor nitens (Acari: Ixodidae) larvae. Parasitol Res 111:1295–1300. https://doi.org/10.1007/s00436-012-2964-0
Dey S, Sinha B, Kalita J (2005) Effect of Eupatorium adenophorum Spreng leaf extracts on the mustard aphid, Lipaphis erysimi Kalt: a scanning electron microscope study. Microsc Res Tech 66:31–36. https://doi.org/10.1002/jemt.20140
Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and B. microplus: laboratory tests of insecticides. J Econ Entomol 66:130–133. https://doi.org/10.1093/jee/66.1.130
Elango G, Rahuman AA, Zahir AA, Kamaraj C, Bagavan A, Rajakumar G, Jayaseelan C, Santhoshkumar T, Marimuthu S (2010) Evaluation of repellent properties of botanical extracts against Culex tritaeniorhynchus Giles (Diptera: Culicidae). Parasitol Res 107:577–584. https://doi.org/10.1007/s00436-010-1897-8
Ellse L, Wall R (2014) The use of essential oils in veterinary ectoparasite control: a review. Med Vet Entomol 28:233–243. https://doi.org/10.1111/mve.12033
Finney D (1964) Probit analysis: a statistical treatment of the sigmoid response curve. University Press, Cambridge
Garcia MV, Matias J, Barros JC, de Lima DP, Lopes RS, Andreotti R (2012) Chemical identification of Tagetes minuta Linnaeus (Asteraceae) essential oil and its acaricidal effect on ticks. Rev Bras Parasitol Vet 21:405–411. https://doi.org/10.1590/S1984-29612012000400011
Gazim ZC, Demarchi IG, Lonardoni MVC, Amorim ACL, Hovell AMC, Rezende CM, Ferreira GA, de Lima EL, de Cosmo FA, Cortez DAG (2011) Acaricidal activity of the essential oil from Tetradenia riparia (Lamiaceae) on the cattle tick Rhipicephalus (Boophilus) microplus (Acari; Ixodidae). Exp Parasitol 129:175–178. https://doi.org/10.1016/j.exppara.2011.06.011
Godara R, Parveen S, Katoch R, Yadav A, Verma PK, Katoch M, Kaur D, Ganai A, Raghuvanshi P, Singh NK (2014) Acaricidal activity of extract of Artemisia absinthium against Rhipicephalus sanguineus of dogs. Parasitol Res 113:747–754. https://doi.org/10.1007/s00436-013-3704-9
Gomes GA, Monteiro CM, Senra TO, Zeringota V, Calmon F, Matos RS, Daemon E, Gois RW, Santiago GM, de Carvalho MG (2012) Chemical composition and acaricidal activity of essential oil from Lippia sidoides on larvae of Dermacentor nitens (Acari: Ixodidae) and larvae and engorged females of Rhipicephalus microplus (Acari: Ixodidae). Parasitol Res 111:2423–2430. https://doi.org/10.1007/s00436-012-3101-9
Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pestic Biochem Physiol 99:200–207. https://doi.org/10.1016/j.pestbp.2010.12.005
Hanifah AL, Awang SH, Ming HT, Abidin SZ, Omar MH (2011) Acaricidal activity of Cymbopogon citratus and Azadirachta indica against house dust mites. Asian Pac J Trop Biomed 1:365–369. https://doi.org/10.1016/S2221-1691(11)60081-6
Heath A (2016) Biology, ecology and distribution of the tick, Haemaphysalis longicornis Neumann (Acari: Ixodidae) in New Zealand. N Z Vet J 64:10–20. https://doi.org/10.1080/00480169.2015.1035769
Heimerdinger A, Olivo CJ, Molento MB, Agnolin CA, Ziech MF, Scaravelli LF, Skonieski FR, Both JF, Charao PS (2006) Alcoholic extract of lemongrass (Cymbopogon citratus) on the control of Boophilus microplus in cattle. Rev Bras Parasitol Vet 15:37–39
Higa LDOS, Garcia MV, Rodrigues VDS, Junior PB, Barradas Pina FT, Barros JC, Andreotti R (2019) Effects of cypermethrin, chlorpyrifos and piperonyl butoxide-based pour-on and spray acaricides on controlling the tick Rhipicephalus microplus. Syst Appl Acarol 24:278–286. https://doi.org/10.11158/saa.24.2.10
Ikadai H, Sasaki M, Ishida H, Matsuu A, Igarashi I, Fujisaki K, Oyamada T (2007) Molecular evidence of Babesia equi transmission in Haemaphysalis longicornis. Am J Trop Med Hyg 76:694–697
Izzo MM, Poe I, Horadagoda N, De Vos AJ, House JK (2010) Haemolytic anaemia in cattle in NSW associated with Theileria infections. Aust Vet J 88:45–51. https://doi.org/10.1111/j.1751-0813.2009.00540.x
Jaenson TGT, Garboui S, Pålsson K (2006) Repellency of oils of lemon eucalyptus, geranium, and lavender and the mosquito repellent mygga natural to Ixodes ricinus (Acari: Ixodidae) in the laboratory and field. J Med Entomol 43:731–736. https://doi.org/10.1093/jmedent/43.4.731
Jiang J, An H, Lee JS, O’Guinn ML, Kim HC, Chong ST, Zhang Y, Song D, Burrus RG, Bao Y, Klein TA, Richards AL (2018) Molecular characterization of Haemaphysalis longicornis-borne rickettsiae, Republic of Korea and China. Ticks Tick Borne Dis 9:1606–1613. https://doi.org/10.1016/j.ttbdis.2018.07.013
Jõgar K, Kuusik A, Metspalu L, Hiiesaar K, Grishakova M, Luik A (2008) Effects of neem ec on gas exchange, tracheal ventilation, and water loss in diapausing pupae of Pieris brassicae. Entomol Exp Appl 126:165–173. https://doi.org/10.1111/j.1570-7458.2007.00648.x
Karunamoorthi K, Ilango K (2010) Larvicidal activity of Cymbopogon citratus (DC) stapf. and Croton macrostachyus Del. against Anopheles arabiensis Patton, a potent malaria vector. Eur Rev Med Pharmacol Sci 14:57–62
Karunamoorthi K, Ilango K, Murugan K (2010) Laboratory evaluation of traditionally used plant-based insect repellent against the malaria vector Anopheles arabiensis Patton (Diptera: Culicidae). Parasitol Res 106:1217–1223. https://doi.org/10.1007/s00436-010-1797-y
Kiss T, Cadar D, Spinu M (2012) Tick prevention at a crossroad: new and renewed solutions. Vet Parasitol 187:357–366. https://doi.org/10.1016/j.vetpar.2012.02.010
Liu J, Liu Z, Zhang Y, Yang X, Gao Z (2005) Biology of Dermacentor silvarum (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 36:131–138
Liu H, Li Q, Zhang X, Li Z, Wang Z, Song M, Wei F, Wang S, Liu Q (2016) Characterization of rickettsiae in ticks in northeastern China. Parasit Vectors 9:498–498. https://doi.org/10.1186/s13071-016-1764-2
Muyobela J, Nkunika PO, Mwase ET (2016) In vitro acaricidal activity of Bobgunnia madagascariensis Desv. against Amblyomma variegatum (Fabricius) (Acari: Ixodidae). Trop Anim Health Prod 48:625–631. https://doi.org/10.1007/s11250-016-1009-6
Neville AC (2012) Biology of the arthropod cuticle. Springer, Berlin
Noh Y, Lee YS, Kim HC, Chong ST, Klein TA, Jiang J, Richards AL, Lee HK, Kim SY (2017) Molecular detection of Rickettsia species in ticks collected from the southwestern provinces of the Republic of Korea. Parasit Vectors 10:20. https://doi.org/10.1186/s13071-016-1955-x
Nong X, Ren YJ, Wang JH, Fang CL, Xie Y, Yang DY, Liu TF, Chen L, Zhou X, Gu XB, Zheng WP, Peng XR, Wang SX, Lai SJ, Yang GY (2013) Clinical efficacy of botanical extracts from Eupatorium adenophorum against the scab mite, Psoroptes cuniculi. Vet Parasitol 192:247–252. https://doi.org/10.1016/j.vetpar.2012.10.005
Nong X, Tan YJ, Wang JH, Xie Y, Fang CL, Chen L, Liu TF, Yang DY, Gu XB, Peng XR, Wang SX, Yang GY (2013) Evaluation acaricidal efficacy of botanical extract from Eupatorium adenophorum against the hard tick Haemaphysalis longicornis (Acari: Ixodidae). Exp Parasitol 135:558–563. https://doi.org/10.1016/j.exppara.2013.09.001
Oliveira RA, Roat TC, Carvalho SM, Malaspina O (2014) Side-effects of thiamethoxam on the brain and midgut of the africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environ Toxicol 29:1122–1133. https://doi.org/10.1002/tox.21842
Pazinato R, Volpato A, Baldissera MD, Santos RCV, Baretta D, Vaucher RA, Giongo JL, Boligon AA, Stefani LM, Da Silva AS (2016) In vitro effect of seven essential oils on the reproduction of the cattle tick Rhipicephalus microplus. J Adv Res 7:1029–1034. https://doi.org/10.1016/j.jare.2016.05.003
Pinto Z, Sánchez FF, Dos Santos AR, Amaral AC, Ferreira J, Escalona-Arranz JC, Queiroz M (2015) Chemical composition and insecticidal activity of Cymbopogon citratus essential oil from Cuba and Brazil against housefly. Rev Bras Parasitol Vet 24:36–44. https://doi.org/10.1590/S1984-29612015006
Pushpanathan T, Jebanesan A, Govindarajan M (2006) Larvicidal, ovicidal and repellent activities of Cymbopogan citratus Stapf (Graminae) essential oil against the filarial mosquito Culex quinquefasciatus (Say) (Diptera: Culicidae). Trop Biomed 23:208–212. https://doi.org/10.1016/j.trstmh.2006.03.010
Rahuman AA, Gopalakrishnan G, Venkatesan P, Geetha K (2008) Larvicidal activity of some euphorbiaceae plant extracts against Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 102:867–873. https://doi.org/10.1007/s00436-007-0839-6
Rainey T, Occi J, Robbins R, Egizi A (2018) Discovery of Haemaphysalis longicornis (Ixodida: Ixodidae) parasitizing a sheep in New Jersey, United States. J Med Entomol 55:1–3. https://doi.org/10.1093/jme/tjy006
Rodriguez-Vivas RI, Jonsson NN, Bhushan C (2018) Strategies for the control of Rhipicephalus microplus ticks in a world of conventional acaricide and macrocyclic lactone resistance. Parasitol Res 117:3–29. https://doi.org/10.1007/s00436-017-5677-6
Rosado-Aguilar JA, Aguilar-Caballero A, Rodriguez-Vivas RI, 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). Vet Parasitol 168:299–303. https://doi.org/10.1016/j.vetpar.2009.11.022
Sibul I, Kuusik A, Voolma K (2004) Monitoring of gas exchange cycles and ventilatory movements in the pine weevil Hylobius abietis: respiratory failures evoked by a botanical insecticide. Entomol Exp Appl 110:173–179. https://doi.org/10.1111/j.0013-8703.2004.00134.x
Stone BF, Haydock KP (1962) A method for measuring the acaricide-susceptibility of the cattle tick Boophilus microplus (can.). Bull Entomol Res 53:563–578. https://doi.org/10.1017/S000748530004832X
Tabara K, Kawabata H, Arai S, Itagaki A, Yamauchi T, Katayama T, Fujita H, Takada N (2011) High incidence of rickettsiosis correlated to prevalence of Rickettsia japonica among Haemaphysalis longicornis tick. J Vet Med Sci 73:507–510. https://doi.org/10.1292/jvms.10-0369
Talactac MR, Yoshii K, Hernandez EP, Kusakisako K, Galay RL, Fujisaki K, Mochizuki M, Tanaka T (2017) Synchronous langat virus infection of Haemaphysalis longicornis using anal pore microinjection. Viruses 9:189. https://doi.org/10.3390/v9070189
Teng K, Jiang Z (1991) Economic insect fauna of China. Science Press, Beijing
Wu XB, Na RH, Wei SS, Zhu JS, Peng HJ (2013) Distribution of tick-borne diseases in China. Parasit Vectors 6:119. https://doi.org/10.1186/1756-3305-6-119
Yu Z, Wang H, Wang T, Sun W, Yang X, Liu J (2015) Tick-borne pathogens and the vector potential of ticks in China. Parasit Vectors 8:24. https://doi.org/10.1186/s13071-014-0628-x
Yun SM, Lee WG, Ryou J, Yang SC, Park SW, Roh JY, Lee YJ, Park C, Han MG (2014) Severe fever with thrombocytopenia syndrome virus in ticks collected from humans, South Korea, 2013. Emerg Infect Dis 20:1358–1361. https://doi.org/10.3201/eid2008.131857
Yun SM, Lee YJ, Choi W, Kim HC, Chong ST, Chang KS, Coburn JM, Klein TA, Lee WJ (2016) Molecular detection of severe fever with thrombocytopenia syndrome and tick-borne encephalitis viruses in ixodid ticks collected from vegetation, Republic of Korea, 2014. Ticks Tick Borne Dis 7:970–978. https://doi.org/10.1016/j.ttbdis.2016.05.003
Zahir AA, Rahuman AA, Bagavan A, Santhoshkumar T, Mohamed RR, Kamaraj C, Rajakumar G, Elango G, Jayaseelan C, Marimuthu S (2010) Evaluation of botanical extracts against Haemaphysalis bispinosa Neumann and Hippobosca maculata Leach. Parasitol Res 107:585–592. https://doi.org/10.1007/s00436-010-1898-7
Acknowledgements
This project was supported by National Natural Science Foundation of China (Grant No. 31272372), the Youth Top Talent Support Program of Hebei Province to Zhijun Yu (Grant No. 2018-2020), the Natural Science Foundation of Hebei Province (Grant No. C2019205064), the Financial Assistance for the Introduction of Overseas Researchers (Grant No. C20190350), the High level talent support project of Hebei Province (Grant No. A201901031) and the Science Foundation of Hebei Normal University (Grant No. L2018J04). Desmond O. Agwunobi was supported by the China Scholarship Council (CSC). The authors thank Hu Yuhong, Wang Duo, Dr. Wang Hui, and Dr. Abolfazl Masoudi for their technical support. We also acknowledge provision of the essential oil by AYUS-Oshadhi Hautpflege (Bühl, Germany).
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Agwunobi, D.O., Pei, T., Wang, K. et al. Effects of the essential oil from Cymbopogon citratus on mortality and morphology of the tick Haemaphysalis longicornis (Acari: Ixodidae). Exp Appl Acarol 81, 37–50 (2020). https://doi.org/10.1007/s10493-020-00485-3
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DOI: https://doi.org/10.1007/s10493-020-00485-3