Anointing Chemicals and Hematophagous Arthropods: Responses by Ticks and Mosquitoes to Citrus (Rutaceae) Peel Exudates and Monoterpene Components

Journal of Chemical Ecology

Volumn 37, Issue 4, 2011, Pages 348-359

  Weldon, Paul J ^a   Carroll, John F ^b   Kramer, Matthew ^b   Bedoukian, Robert H ^c   Coleman, Russell E ^d   Bernier, Ulrich R ^e  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c Bedoukian Research Inc   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^e CENTER FOR MEDICAL   (United States)

Author keywords

Anointing; Citrus; Ectoparasites; Monoterpenes; Mosquitoes; Repellent; Ticks

Indexed keywords

ACETIC ACID DERIVATIVE; GERANIOL; GERANYL ACETATE; INSECT REPELLENT; TERPENE;

BEHAVIORAL ECOLOGY; ECTOPARASITE; EXUDATION; FRUIT; MONOTERPENE; MOSQUITO; REPELLENT; TICK;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOASSAY; CHEMISTRY; CITRUS; DRUG EFFECT; ECTOPARASITOSIS; FEEDING BEHAVIOR; FEMALE; FRUIT; GAS CHROMATOGRAPHY; METHODOLOGY; MOSQUITO; NYMPH; PHYSIOLOGY; TICK; VOLATILIZATION;

ACETATES; ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL ASSAY; CHROMATOGRAPHY, GAS; CITRUS; CULICIDAE; ECTOPARASITIC INFESTATIONS; FEEDING BEHAVIOR; FEMALE; FRUIT; INSECT REPELLENTS; MONOTERPENES; NYMPH; TERPENES; TICKS; VOLATILIZATION;

AEDES AEGYPTI; AMBLYOMMA; AMBLYOMMA AMERICANUM; ANIMALIA; ARTHROPODA; AVES; CITRUS; CITRUS LIMON; IXODIDA; MAMMALIA; RUTACEAE; VERTEBRATA;

EID: 79954987573     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-011-9922-7     Document Type: Article

References (63)

1. Anaso, H. U., Ilouno, L. E, Onuorah, D., and Umerie, S. C. 1990. Potency of orange peels as a mosquito fumigant. Biol. Wastes 34: 83-88.
2. Arias, B. A., and Ramón-Laca, L. 2005. Pharmacological properties of citrus and their ancient and medieval uses in the Mediterranean region. J. Ethnopharmacol. 97: 89-95.
3. Baker, M. 1996. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38: 263-270.
4. Bernier, U. R., Kline, D. L., and Posey, K. H. 2007a. Human emanations and related natural compounds that inhibit mosquito host-finding abilities, pp. 77-100, in M. Debboun, S. P. Frances, and D. Strickman (eds.). Insect Repellents: Principles, Methods, and Uses. CRC, Boca Raton.
5. Bernier, U. R., Kline, D. L., Allan, S. A., and Barnard, D. R. 2007b. Laboratory comparison of Aedes aegypti attraction to human odors and to synthetic human odor compounds and blends. J. Am. Mosq. Control Assoc. 23: 288-293.
6. Blum, M. S. 1981. Chemical Defenses of Arthropods. Academic, New York.
7. Buckley, J. S. 1983. The Feeding Behavior, Social Behavior, and Ecology of the White-Faced Monkey, Cebus capucinus, at Trujillo, Northern Honduras, Central America. Ph. D. Dissertation, University of Texas, Austin.
8. Bunker, C. W. O., and Hirschfelder, A. D. 1925. Mosquito repellents. Am. J. Trop. Med. 5: 359-383.
9. Butler, J. F. 2007. Use of olfactometers for determining attractants and repellents, pp. 161-194, in M. Debboun, S. P. Frances, and D. Strickman (eds.). Insect Repellents: Principles, Methods, and Uses. CRC, Boca Raton.
10. Calabrese, F. 2002. Origin and history, pp. 1-15, in G. Dugo and A. Di Giacomo (eds.). Citrus: The Genus Citrus. Taylor & Francis, New York.
11. Campbell, C. J. 2000. Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama. Am. J. Primatol. 51: 205-208.
12. Carroll, J. F. 1994. Feeding deterrence of northern fowl mites (Acari: Macronyssidae) by some naturally occurring plant substances. Pest. Sci. 41: 203-207.
13. Carroll, J. F., Kramer, M., Weldon, P. J., and Robbins, R. G. 2005. Anointing chemicals and ectoparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma americanum. J. Chem. Ecol. 31: 63-75.
14. Choi, W.-S., Park, B.-S., Ku, S.-K., and Lee, S.-E. 2002. Repellent activities of essential oils and monoterpenes against Culex pipiens pallens. J. Am. Mosq. Control Assoc. 18: 348-351.
15. Chungsamarnyart, N., and Jansawan, W. 1996. Acaricidal activity of peel oil of Citrus spp. on Boophilus microplus. Kasetsart J. (Nat. Sci.) 30: 112-117.
16. Clayton, D. H., and Vernon, J. G. 1993. Common grackle anting with lime fruit and its effect on ectoparasites. Auk 110: 951-952.
17. Dejoseph, M., Taylor, R. S. L., Baker, M., and Aregullin, M. 2002. Fur-rubbing behavior of capuchin monkeys. J. Am. Acad. Dermatol. 46: 924-925.
18. Del Fabbro, S., and Nazzi, F. 2008. Repellent effect of sweet basil compounds on Ixodes ricinus ticks. Exp. Appl. Acarol. 45: 219-228.
19. Dietrich, G., Dolan, M. C., Peralta-Cruz, J., Schmidt, J., Piesman, J., Eisen, R. J., and Karchesy, J. J. 2006. Repellent activity of fractionated compounds from Chamaecyparis nootkatensis essential oil against nymphal Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 43: 957-961.
20. Don-Pedro, K. N. 1996. Investigation of single and joint fumigant insecticidal action of citruspeel oil components. Pest. Sci. 46: 79-84.
21. Dugo, G., Cotroneo, A., Verzera, A., and Bonaccorsi, I. 2002. Composition of the volatile fraction of cold-pressed citrus peel oils, pp. 201-317, in G. Dugo and A. Di Giacomo (eds.). Citrus: The Genus Citrus. Taylor & Francis, New York.
22. Falótico, T., Labruna, M. B., Verderane, M. P., De Resende, B. D., Izar, P., and Ottoni, E. B. 2007. Repellent efficacy of formic acid and the abdominal secretion of carpenter ants (Hymenoptera: Formicidae) against Amblyomma ticks (Acari: Ixodidae). J. Med. Entomol. 44: 718-721.
23. Gillij, Y. G., Gleiser, R. M., and Zygadlo, J. A. 2008. Mosquito repellent activity of essential oils of aromatic plants growing in Argentina. Bioresour. Technol. 99: 2507-2515.
24. Hao, H., Wei, J., Dai, J., and Du, J. 2008. Host-seeking and blood-feeding behavior of Aedes albopictus (Diptera: Culicidae) exposed to vapors of geraniol, citral, citronellal, eugenol, or anisaldehyde. J. Med. Entomol. 45: 533-539.
25. Hink, W. F., Liberati, T. A., and Collart, M. G. 1988. Toxicity of linalool to life stages of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae), and its efficacy in carpet and on animals. J. Med. Entomol. 25: 1-4.
26. Hwang, Y.-S., Wu, K.-H., Kumamoto, J., Axelrod, H., and Mulla, M. S. 1985. Isolation and identification of mosquito repellents in Artemisia vulgaris. J. Chem. Ecol. 11: 1297-1306.
27. Ibrahim, M. A., Kainulainen, P., Aflatuni, A., Tiilikkala, K., and Holopainen, J. K. 2001. Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agr. Food Sci. Finland 10: 243-259.
28. Johnson, C. 1971. Grackles (Quiscalus quiscula) use lemon oil for anting. Fla. Nat. 44: 123.
29. Karlberg, A.-T., Magnusson, K., and Nilsson, U. 1992. Air oxidation of d-limonene (the citrus solvent) creates potent allergens. Contact Dermat. 26: 332-340.
30. Kline, D. L., Bernier, U. R., Posey, K. H., and Barnard, D. R. 2003. Olfactometric evaluation of spatial repellents for Aedes aegypti. J. Med. Entomol. 40: 463-467.
31. Koh, D., and Ong, C.-N. 1999. Phytophotodermatitis due to the application of Citrus hystrix as a folk remedy. Br. J. Dermatol. 140: 737-738.
32. Kramer, M., Weldon, P. J., and Carroll, J. F. 2009. Composite scores for concurrent behaviours constructed using canonical discriminate analysis. Anim. Behav. 77: 763-768.
33. Laskey, A. R. 1948. Bronzed grackle anointing plumage with orange-skin. Wilson Bull. 60: 244-245.
34. Leca, J.-B., Gunst, N., and Petit, O. 2007. Social aspects of fur-rubbing in Cebus capucinus and C. apella. Int. J. Primatol. 28: 801-817.
35. Lee, S., Tsao, R., Peterson, C., and Coats, J. R. 1997. Insecticidal activity of monoterpenoids to western corn rootworm (Coleoptera: Chrysomelidae), twospotted spider mite (Acari: Tetranychidae), and house fly (Diptera: Muscidae). J. Econ. Entomol. 90: 883-892.
36. Logan, J. G., Seal N. J., Cook, J. I., Stanczyk, N. M., Birkett, M. A., Clark S. J., Gezan, S. A., Wadhams, L. J., Pickett, J. A., and Mordue (Luntz), A. J. 2009. Identification of human-derived volatile chemicals that interfere with attraction of the Scottish biting midge and their potential use as repellents. J. Med. Entomol. 46: 208-219.
37. Lota, M. -L., De Rocca Serra, D., Tomi, F., Jacquemond, C., and Casanova, J. 2002. Volatile components of peel and leaf oils of lemon and lime species. J. Agric. Food Chem. 50: 796-805.
38. Lwande, W., Ndakala, A. J., Hassanali, A., Moreka, L., NyandaT, E., Ndungu, M., Amiani, H., Gitu, P. M., Malonza, M. M., and Punyua, D. K. 1999. Gynandropsis gynandra essential oil and its constituents as tick (Rhipicephalus appendiculatus) repellents. Phytochemistry 50: 401-405.
39. Müller, G. C., Junnila, A., Butler, J., Kravchenko, V. D., Revay, E. E., Weiss, R. W., and Schlein, Y. 2009. Efficacy of the botanical repellents geraniol, linalool, and citronella against mosquitoes. J. Vector Ecol. 34: 2-8.
40. Ndungu, M., Lwande, W., Hassanali, A., Moreka, L., and Chhabra, S. C. 1995. Cleome monophylla essential oil and its constituents as tick (Rhipicephalus appendiculatus) and maize weevil (Sitophilus zeamais) repellents. Entomol. Exp. Appl. 76: 217-222.
41. Pälsson, K., Jaenson, T. G. T., Bæckström, P., and Borg-Karlson, A.-K. 2008. Tick repellent substances in the essential oil of Tanacetum vulgare. J. Med. Entomol. 45: 88-93.
42. Park, B.-S., Choi, W.-S., Kim, J.-H., Kim, K.-H., and Lee, S.-E. 2005. Monoterpenes from thyme (Thymus vulgaris) as potential mosquito repellents. J. Am. Mosq. Control Assoc. 21: 80-83.
43. Perrucci, S., Macchioni, G., Cioni, P. L., Flamini, G., and Morelli, I. 1995. Structure/activity relationship of some natural monoterpenes as acaricides against Psoroptes cuniculi. J. Nat Prod. 58: 1261-1264.
44. Posey, K. H., Barnard, D. R., and Schreck, C. E. 1998. Triple cage olfactometer for evaluating mosquito (Diptera: Culicidae) attraction responses. J. Med. Entomol. 35: 330-334.
45. Prates, H. T., Leite, R. C., Craveiro, A. A., and Oliveira, A. B. 1998. Identification of some chemical components of the essential oil from molasses grass (Melinis minutiflora Beauv.) and their activity against cattle-tick (Boophilus microplus). J. Braz. Chem. Soc. 9: 193-197.
46. Richard, A. 1970. A comparative study of the activity patterns and behavior of Alouatta villosa and Ateles geoffroyi. Folia Primatol. 12: 241-263.
47. Safra, V., Zerba E. N., and Alzogaray, R. A. 2009. Fumigant insecticidal activity and repellent effect of five essential oils and seven monoterpenes on first-instar nymphs of Rhodnius prolixus. J. Med. Entomol. 46: 511-515.
48. Sick, H. 1993. Birds in Brazil: A Natural History. Princeton University Press, Princeton, New Jersey.
49. Stresemann, E. 1935. Die Benutzung von Ameisen zur Gefiederpflege. Ornith. Monatsber. 43: 134-138.
50. Sukumar, K., Perich, M. J., and Boobar, L. R. 1991. Botanical derivatives in mosquito control: a review. J. Am. Mosq. Control Assoc. 7: 210-217.
51. Thorsell, W., Mikiver, A., and Tunón, H. 2006. Repelling properties of some plant materials on the tick Ixodes ricinus L. Phytomedicine 13: 132-134.
52. Toloza, A. C., Zygadlo, J., Cueto, G. M., Biurrun, F., Zerba, E., and Picollo, M. I. 2006. Fumigant and repellent properties of essential oils and component compounds against permethrin-resistant Pediculus humanus capitis (Anoplura: Pediculidae) from Argentina. J. Med. Entomol. 43: 889-895.
53. Traboulsi, A. F., El-Haj, S., Tueni, M., Taoubi, K., Nader, N. A., and Mrad, A. 2005. Repellency and toxicity of aromatic plant extracts against mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Manag. Sci. 61: 597-604.
54. Traina, O., Cafarchia, C., Capelli, G., Iacobellis, N. S., and Otranto, D. 2005. In vitro acaricidal activity of four monoterpenes and solvents against Otodectes cynotis (Acari: Psoroptidae). Exp. Appl. Acarol. 37: 141-146.
55. Tunón, H., Thorsell, W., Mikiver, A., and Malander, I. 2006. Arthropod repellency, especially tick (Ixodes ricinus), exerted by extract from Artemisia abrotanum and essential oil from flowers of Dianthus caryophyllum. Filoterapia 77: 257-261.
56. Vartak, P. H., and Sharma, R. N. 1993. Vapour toxicity & repellence of some essential oils & terpenoids to adults of Aedes aegypti (L.) (Diptera: Culicidae). Indian J. Med. Res. 97: 122-127.
57. Waladde, S. M., and Rice, M. J. 1982. The sensory basis for tick feeding behaviour, pp. 71-118, in F. D. Obenchain and R. Galun (eds.). Physiology of Ticks. Pergamon, New York.
58. Waliwitiya, R., Kennedy, C. J., and Lowenberger, C. A. 2009. Larvicidal and oviposition-altering activity of monoterpenoids, trans-anethole and rosemary oil to the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). Pest Manag. Sci. 65: 241-248.
59. Weldon, P. J., and Carroll, J. F. 2007. Vertebrate chemical defense: secreted and topically acquired deterrents of arthropods, pp. 47-75, in M. Debboun, S. P. Frances, and D. Strickman (eds.). Insect Repellents: Principles, Methods, and Uses. CRC, Boca Raton.
60. Weldon, P. J., Kramer, M., Gordon, S., Spande, T. F., and Daly, J. W. 2006. A common pumiliotoxin from poison frogs exhibits enantioselective toxicity against mosquitoes. Proc. Natl. Acad. Sci., U. S. A. 103: 17818-17821.
61. Whitaker, L. M. 1957. A resumé of anting, with particular reference to a captive orchard oriole. Wilson Bull. 69: 195-262.
62. Zaki, Z. M., Ali, N. A. M., Ahmad, A. S., Zoll, M. F., Hassan, P. H., Jamil, I. K. M., and Bakar, S. A. A. 2005. Four monoterpene compounds: repellency evaluation against Aedes aegypti. Malaysian J. Sci. 24: 225-228.
63. Zimen, E. 1981. The Wolf: A Species in Danger. Delacorte, New York.