Acaricidal Activity of Artemisia nilagirica Leaves Against Rhipicephalus (Boophilus) annulatus Ticks

Abstract

Since time immemorial, human beings have used various parts of plants in either prevention or treatment of ailments. Plants are rich sources of secondary metabolites such as alkaloids, steroids, terpenoids, flavonoids, and phenolic compounds with a high structural diversity. Many plants/herbs with specific biological activities such as antitumor, antioxidant, anti-inflammatory, antifungal, sedative, and acaricidal activity have been reported. Artemisia nilagirica (C. B. Clarke) Pamp. (Compositae) is a plant traditionally used for insect control in the southern part of India. Previous studies have demonstrated the activity of Artemisia species against pests. The present study thus evaluates the acaricidal activity of crude ethanolic extract of A. nilagirica leaves and its fractions against Rhipicephalus (Boophilus) annulatus. Ticks are ectoparasites that transmit several protozoal, viral, and rickettsial diseases. In south India, R. (B.) annulatus is the commonly observed tick species. Control of these acarine parasites that adversely affect milk and meat production is a tough task. Chemical acaricides such as organophosphates, synthetic pyrethroids, amitraz, and ivermectin are commonly used in tick control. The high cost, environmental hazards, and development of acaricidal resistance are some of the drawbacks of these chemical acaricides. Plant-based formulations are one of the promising approaches for the control of ectoparasites. Previously, extracts from various medicinal/aromatic plants were reported for acaricidal activity from our laboratory, such as Tetrastigma leucostaphylum (Dennst.) Alston, Chassalia curviflora (Wall.) Thwaites, Jatropha curcas L., and Ageratum conyzoides Hieron. Biochemical quantification, fluorescence analysis, and primary phytochemical analysis are already reported for the ethanolic extract and its fractions of areal parts of A. nilagirica. Phytochemical characterization of ethanolic extract of A. nilagirica from Kerala, India was shown to have the presence of terpenoids, flavonoids, steroids, saponins, fixed oils and fats, tannins, and glycosides.

Key words

Artemisia nilagirica - Compositae - acaricidal activity - GC-MS - dermal toxicity - wound healing - oral toxicity

• References

• 1 Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 2003; 64: 3-19
• 2 Prashant T, Bimlesh K, Kaur M, Kaur G, Harleen K. Phytochemical screening and extraction: A Review. Internat Pharmaceut Scienc 2011; 1: 98-106
• 3 Kordali S, Aslan I, Calmasur O, Cakir A. Toxicity of essential oils isolated from three Artemisia species and some of their major components to granary weevil, Sitophilus granarius (L.) (Coleoptera: Curculinonidae). Indian Crops Prod 2006; 23: 162-170
• 4 Kim DK, Park JD, Kim SG, Kuk H, Jang MS, Kim SS. Screening of some crude plant extracts for their acaricidal and insecticidal efficacies. J Asia-Pacific Entomol 2005; 8: 93-100
• 5 Felicio JD, Soares LB, Felicio RC, Gonçalez E. Artemisia species as potential weapon against agents and agricultural pests. Curr Biotechnol 2012; 3: 249-257
• 6 Ribeiro VL, dos Santos JC, Martins JR, Schripsema J, Siqueira IR, von Poser GL, Apel MA. Acaricidal properties of the essential oil and precocene II obtained from Calea serrata (Asteraceae) on the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Vet Parasitol 2011; 179: 195-198
• 7 Wall R, Shearer D. Veterinary Entomology. London: Chappman and Hall; 1997: 97-140
• 8 Ghosh S, Azhahianambi P, Yadav MP. Upcoming and future strategies of tick control: a review. J Vector Borne Dis 2007; 44: 79-89
• 9 Food and Agriculture Organization of the United Nations (FAO). Resistance Management and Integrated Parasite Control in Ruminants–Guidelines, Module 1. Ticks: Acaricide Resistance: Diagnosis, Management and Prevention. Rome: FAO, Animal Production and Health Division; 2004: 53
• 10 Agnolin CA, Olivo CJ, Leal MLR, Beck RCR, Meinerz GR, Parra CLC, Machado PR, Foletto V, Bem CM, Nicolodi PRSJ. Efficacy of Cymbopogon nardus (Linn) Rendle and citronella oil on controlling bovine ectoparasites. Rev Bras Plant Med 2010; 1: 482-487
• 11 Krishna TP, Krishna TP, Chithra ND, Deepa PE, Darsana U, Sreelekha KP, Juliet S, Nair SN, Ravindran R, Kumar KG, Ghosh S. Acaricidal activity of petroleum ether extract of leaves of Tetrastigma leucostaphylum (Dennst.) Alston against Rhipicephalus (Boophilus) annulatus . Scientific World J 2014; 2014: 715481
• 12 Palayullaparambil AKT, Palayullaparambil AKT, Juliet S, Renganathan K, Raju R, Athalathil S, Ravindran R, Chandrashekar L, Nair SN, Ghosh S. Pharmaco-chemical characterization and acaricidal activity of ethanolic extract of Chassalia curviflora (Wall ex Kurz.) Thwaites. Pharmacogn J 2016; 8: 215-219
• 13 Juliet S, Reghu R, Sunil AR, Ajith KKG, Suresh NN, Amithamol KK, Amitabh B, Ajay KSR, Srikant G. Jatropha curcas (Linn) leaf extract a possible alternative for population control of Rhipicephalus (Boophilus) annulatus . Asian Pac J Trop Dis 2012; 2: 225-229
• 14 Nair SN, Juliet S, Amithamol KK, Sunil AR, Palayullaparambil AKT, Sreelekha K, Divya TM, Udayan D, Kumar KGA, Ghosh S, Ravindran R. In vitro acaricidal effects of ethanolic extract and its fractions of Ageratum conyzoides L. against common cattle tick, Rhipicephalus (Boophilus) annulatus . Ann Phytomed 2017; 6: 162-168
• 15 Udayan D, Palayullaparambil AKT, Palayullaparambil AKT, Nair SN, Juliet S, Ravindran R, Pradeep AK. Biochemical quantification, fluorescence analysis and phytochemical evaluation of ethanolic extract and its fractions of areal parts of Artemisia nilagirica found in Western Ghats (Wayanad region) of Kerala, India. Pharmacie Globale 2014; 5: 1-8
• 16 Ramachandran PD, Juliet S, Mahesh DM, Drisya K, Adarsh Krishna TP, Sunil AR, Suresh NN, Ajith Kumar KG, Ravindran R, Sujith S, Nisha AR, Suja Rani S, Ranjith D. Pharmaco-chemical characterization of terpenoid fraction of Artemisia nilagirica (Clarke) Pamp. from Western Ghats of Wayanad region of Kerala, India. J Pharmacogn Phytochem 2019; 8: 1343-1348
• 17 Shafi PM, Geetha MKN, Robin AC, Sarma YR, Veena SS. Composition and antifungal activity of the oil of Artemisia nilagirica (Clarke) Pamp. J Essent Oil Res 2004; 16: 377-379
• 18 Haider F, Naqvi AA, Bagchi GD. Oil constituents of Artemisia nilagirica var. septentrionalis during different growth phases at subtropical conditions of North Indian plains. J Essent Oil Res 2007; 19: 5-7
• 19 Badoni R, Semwal DK, Rawat U. Altitudinal variation in the volatile constituents of Artemisia nilagirica . Int J Essen Oil Ther 2009; 3: 66-68
• 20 Sati SC, Sati N, Ahluwalia V, Walia S, Sati OP. Chemical composition and antifungal activity of Artemisia nilagirica essential oil growing in northern hilly areas of India. Nat Prod Res 2012; 27: 45-48
• 21 Sreeram S, Parida R, Sahoo S, Nayak S, Mohanty S. High radical scavenging activity of camphor rich Artemisia nilagirica essential oil growing in eastern plain areas of India. Res J Biotech 2014; 9: 63-65
• 22 Chiasson H, Belanger A, Bostanian N, Vincent C, Poliquin A. Acaricidal properties of Artemisia absinthium and Tanacetum vulgare (Asteraceae) essential oils obtained by three methods of extraction. J Econ Entomol 2001; 94: 167-171
• 23 Tunon H, Thorsell W, Mikiver A, Malander I. Arthropod repellency, especially tick (Ixodes ricinus), exerted by extract from Artemisia abrotanum and essential oil from flowers of Dianthus caryophyllum . Fitoterapia 2006; 77: 257-261
• 24 Pallson K, Jaenson TGT, Ckstrom PB, Borg-Karlson AK. Tick repellent substances in the essential oil of Tanacetum vulgare . J Med Entomol 2008; 45: 88-93
• 25 Cetin H, Cilek JE, Oz E, Aydin L, Deveci O, Yanikoglu A. Acaricidal activity of Satureja thymbra L. essential oil and its major components, carvacrol and γ-terpinene against adult Hyalomma marginatum (Acari: Ixodidae). Vet Parasitol 2010; 17: 287-290
• 26 Ribeiro VL, dos Santos JC, Bordignon SA, Apel MA, Henriques AT, von Poser GL. Acaricidal properties of the essential oil from Hesperozygis ringens (Lamiaceae) on the cattle tick Riphicephalus (Boophilus) microplus . Bioresour Technol 2010; 101: 2506-2509
• 27 Pereira JR, Famadas KM. The efficiency of extracts of Dahlstedtia pentaphylla (Leguminosae, Papilionoidae, Millettiedae) on Boophilus microplus (Canestrini, 1887) in artificially infested bovines. Vet Parasitol 2006; 142: 192-195
• 28 Fernandes FF, Freitas EPS. Acaricidal activity of an oleoresinous extract from Copaifera reticulata (Leguminosae: Caesalpinioideae) against larvae of the southern cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Vet Parasitol 2007; 147: 150-154
• 29 Magadum S, Mondal DB, Ghosh S. Comparative efficacy of Annona squamosa and Azadirachta indica extracts against Boophilus microplus Izatnagar isolate. Parasitol Res 2009; 105: 1085-1091
• 30 Porter RBR, Reese PB, Williams LAD, Williams DJ. Acaricidal and insecticidal activities of cadina-4,10(15)-dien-3-one. Phytochemistry 1995; 40: 735-738
• 31 Lee CH, Park JM, Song HY, Jeong EY, Lee HS. Acaricidal activities of major constituents of essential oil of Juniperus chinensis leaves against house dust and stored food mites. J Food Prot 2009; 72: 1686-1691
• 32 Oh MS, Yang JY, Kim MG, Lee HS. Acaricidal activities of β-caryophyllene oxide and structural analogues derived from Psidium cattleianum oil against house dust mites. Pest Manag Sci 2014; 70: 757-762
• 33 Duan DD, Bu CY, Cheng J, Wang YN, Shi GL. Isolation and identification of acaricidal compounds in Inula japonica (Asteraceae). J Econ Entomol 2011; 104: 375-378
• 34 McFarlane JE. Fatty acids, methyl esters and insect growth. Comp Biochem Physiol 1968; 24: 377
• 35 Wang YN, Wang HX, Shen ZJ, Zhao LL, Clarke SR, Sun JH, Du YY, Shi GL. Methyl palmitate an acaricidal compound occurring in green walnut husks. J Econ Entomol 2009; 102: 196-202
• 36 Du YH, Li JL, Jia RY, Yin ZQ, Li XT, Ye G, Li Z, Zhang YQ. Acaricidal activity of four fractions and octadecanoic acid-tetrahydrofuran-3,4-diyl ester isolated from chloroform extracts of neem (Azadirachta indica) oil against Sarcoptes scabiei var. cuniculi larvae in vitro . Vet Parasitol 2009; 163: 1-2 175–178
• 37 Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH. Boophilus annulatus and Boophilus microplus: laboratory tests for insecticides. J Econ Entomol 1973; 66: 130-133
• 38 Ravindran R, Juliet S, Ajith Kumar KG, Sunil AR, Suresh N, Nair Amithamol KK, Rawat AKS, Ghosh S. Toxic effects of various solvents against Rhipicephalus (Boophilus) annulatus . Ticks Tick Borne Dis 2011; 2: 160-162
• 39 Ravindran R, Juliet S, Sunil AR, Ajith Kumar KG, Nair SN, Amithamol KK, Bandyopadhyay A, Rawat AKS, Ghosh S. Acaricidal activity of Cassia alata (Linn) on Rhipicephlaus (Boophilus) annulatus . Exp Appl Acarol 2012; 56: 69-74
• 40 Sharma AK, Rinesh K, Sachin K, Gaurav N, Singh NK, Rawat SS, Dhakad ML, Rawat AKS, Ray DD, Ghosh S. Deltamethrin and cypermethrin resistance status of Rhipicephalus (Boophilus) microplus collected from six agro-climatic regions of India. Vet Parasitol 2012; 188: 337-345
• 41 OECD. Test No. 425: acute oral toxicity: up-and-down procedure. OECD Guidelines for the Testing of Chemicals, Section 4. Available at (Accessed October 16, 2008): https://doi.org/10.1787/9789264071049-en
• 42 OECD. Test No. 404: acute dermal irritation/corrosion. OECD Guidelines for the Testing of Chemicals, Section 4. Available at (Accessed April 24, 2002): https://doi.org/10.1787/9789264070622-en
• 43 Draize JH, Woodard G, Calvery HO. Methods for the study of irritation and toxicity of substances applied topically to the skin and mucous membranes. J Pharmacol Exp Ther 1944; 82: 377-390
• 44 OECD. Test No. 410: repeated dose dermal toxicity: 21/28-day study. OECD Guidelines for the Testing of Chemicals, Section 4. Available at (Accessed May 12, 1981): https://doi.org/10.1787/9789264070745-en
• 45 Kokane DD, More RY, Kale MB, Nehete MN, Mehendale PC, Gadgoli CH. Evaluation of wound healing activity of root of Mimosa pudica . J Ethnopharmacol 2009; 124: 311-315