Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T10:57:56.078Z Has data issue: false hasContentIssue false
  • English
  • Français

Varroa destructor (Mesostigmata: Varroidae) electrophysiological activity towards common yarrow (Asteraceae) essential oil and its components

Published online by Cambridge University Press:  26 November 2020

Michael Light Open the ORCID record for Michael Light [Opens in a new window] ,
Nicoletta Faraone Open the ORCID record for Nicoletta Faraone [Opens in a new window] ,
Dave Shutler ,
G. Christopher Cutler  and
N. Kirk Hillier
Michael Light*
Affiliation:
Department of Biology, Acadia University, Wolfville, Nova Scotia, B4P 2R6, Canada
Nicoletta Faraone
Affiliation:
Department of Chemistry, Acadia University, Wolfville, Nova Scotia, B4P 2R6, Canada
Dave Shutler
Affiliation:
Department of Biology, Acadia University, Wolfville, Nova Scotia, B4P 2R6, Canada
G. Christopher Cutler
Affiliation:
Department of Plant, Food, and Environmental Sciences, Dalhousie University, Truro, Nova Scotia, B2N 5E3, Canada
N. Kirk Hillier
Affiliation:
Department of Biology, Acadia University, Wolfville, Nova Scotia, B4P 2R6, Canada
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Essential oils produced by plants are a rich source of metabolites that can have toxic or behaviour-modifying effects on arthropods. Some essential oils have shown promise in management of the mite Varroa destructor Anderson and Trueman (Mesostigmata: Varroidae), a parasite of western honey bees, Apis mellifera Linnaeus (Hymenoptera: Apidae). Essential oil and its components from common yarrow, Achillea millefolium Linnaeus (Asteraceae), are reported to have both insecticidal and repellent properties for other arthropod pests and may have activity against V. destructor. Here, we evaluate responses of V. destructor towards common yarrow essential oil using gas chromatography paired with electrotarsal detection. We identified 38 essential oil components that elicited electrophysiological responses from V. destructor. Components of common yarrow essential oil identified as electrophysiologically active in this study are reported elsewhere as active components of other management strategies for V. destructor infestations (e.g., thyme oil; Thymus sp. (Lamiaceae)). Pending behavioural assessment, the efficacy of common yarrow essential oil in honey bee colonies infested by V. destructor should be explored in field conditions.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 2 , April 2021 , pp. 211 - 221
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Present address: Department of Forestry, University of Toronto, Daniels Faculty of Architecture and Design, Toronto, Ontario, M5S 3B3, Canada

Subject editor: Maya Evenden

References

Ali, A., Radwan, M.M., Wanas, A.S., and Khan, I.A. 2018. Repellent activity of carrot seed essential oil and its pure compound, carotol, against mosquitoes. Journal of the American Mosquito Control Association, 34: 272–280.CrossRefGoogle ScholarPubMed
Bissinger, B.W. and Roe, R.M. 2010. Tick repellents: past, present, and future. Pesticide Biochemistry and Physiology, 96: 63–79.CrossRefGoogle Scholar
Blenau, W., Rademacher, E., and Baumann, A. 2012. Plant essential oils and formamidines as insecticides/acaricides: what are the molecular targets? Apidologie, 43: 334–347.Google Scholar
Calderone, N.W. 1999. Evaluation of formic acid and thymol-based blend of natural products for the fall control of Varroa jacobsoni (Acari: Varroidae) in colonies of Apis mellifera (Hymenoptera: Apidae). Journal of Economic Entomology, 92: 253–260.CrossRefGoogle Scholar
Carroll, M.J. and Duehl, A.J. 2012. Collection of volatiles from honeybee larvae and adults enclosed on brood frames. Apidologie, 43: 715–730.CrossRefGoogle Scholar
Chandler, R.F., Hooper, S.N., and Harvey, M.J. 1982. Ethnobotany and phytochemistry of yarrow, Achillea millefolium, compositae. Economic Botany, 36: 203–223.CrossRefGoogle Scholar
Conchou, L., Lucas, P., Meslin, C., Proffit, M., Staudt, M., and Renou, M. 2019. Insect odorscapes: from plant volatiles to natural olfactory scenes. Frontiers in Physiology, 10: 1–20.CrossRefGoogle ScholarPubMed
Cook, S.M., Khan, Z.R., and Pickett, J.A. 2007. The use of push-pull strategies in integrated pest management. Annual Review of Entomology, 52: 375–400.CrossRefGoogle ScholarPubMed
Currie, R.W., Pernal, S.F., and Guzmán-Novoa, E. 2010. Honey bee colony losses in Canada. Journal of Apicultural Research, 49: 104–106.CrossRefGoogle Scholar
DeGrandi-Hoffman, G., Ahumada, F., and Graham, H. 2017. Are dispersal mechanisms changing the host-parasite relationship and increasing the virulence of Varroa destructor (Mesostigmata: Varroidae) in managed honey bee (Hymenoptera: Apidae) colonies? Environmental Entomology, 46: 737–746.CrossRefGoogle ScholarPubMed
Del Fabbro, S. and Nazzi, F. 2013. From chemistry to behavior: molecular structure and bioactivity of repellents against Ixodes ricinus ticks. PLOS One, 8: 1–9.CrossRefGoogle ScholarPubMed
Dietemann, V., Nazzi, F., Martin, S.J., Anderson, D.L., Locke, B., Delaplane, K.S., et al. 2013. Standard methods for varroa research. Journal of Apicultural Research, 52: 1–54.Google Scholar
Eguaras, M.J., Fuselli, S., Gende, L., Fritz, R., Ruffinengo, S.R., Clemente, G., et al. 2005. An in vitro evaluation of Tagetes minuta essential oil for the control of the honeybee pathogens Paenibacillus larvae and Ascosphaera apis, and the parasitic mite Varroa destructor . Journal of Essential Oil Research, 17: 336–340.CrossRefGoogle Scholar
Enan, E. 2001. Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology. Part C: Toxicology & Pharmacology, 130: 325–337.Google ScholarPubMed
Enan, E. 2005. Molecular response of Drosophila melanogaster tyramine receptor cascade to plant essential oils. Insect Biochemistry and Molecular Biology, 35: 309–321.CrossRefGoogle ScholarPubMed
Ettre, L.S. 1993. Nomenclature for chromatography: IUPAC recommendations 1993. Pure and Applied Chemistry, 65: 819–872.CrossRefGoogle Scholar
Ferland, J., Nasr, M., Wilson, G., Jordan, C., Kempers, M., Kozak, P., et al. 2017. Canadian Association of Professional Apiculturists statement on honey bee wintering losses in Canada [online]. Available from https://capabees.com/shared/2016/07/2017-CAPA-Statement-on-Colony-Losses-r.pdf [accessed 24 September 2020].Google Scholar
González-Gómez, R., Otero-Colina, G., Villanueva-Jiménez, J.A., Pérez-Amaro, J.A., and Soto-Hernández, R.M. 2006. Azadirachta indica toxicity and repellence of Varroa destructor (Acari: Varroidae). Agrociencia, 40: 741–751.Google Scholar
Hanes, M.R. 2015. Response of olfactory neurons in Varroa destructor mites to attractant and repellent semiochemicals [online]. Acadia University, Wolfville, Nova Scotia, Canada. Available from https://scholar.acadiau.ca/islandora/object/theses:1179 [accessed 24 September 2020].Google Scholar
Human, H., Brodschneider, R., Dietemann, V., Dively, G., Ellis, J.D., Forsgren, E., et al. 2013. Miscellaneous standard methods for Apis mellifera research. Journal of Apicultural Research, 52: 1–53.CrossRefGoogle Scholar
Imdorf, A., Bogdanov, S., Ochoa, R.I., and Calderone, N.W. 1999. Use of essential oils for the control of Varroa jacobsoni Oud. in honey bee colonies. Apidologie, 30: 209–228.CrossRefGoogle Scholar
Isman, M.B. 2020. Botanical insecticides in the twenty-first century: fulfilling their promise? Annual Review of Entomology, 65: 233–249.Google ScholarPubMed
Ishaaya, I., Nauen, R., and Horowitz, A.R. 2007. Insecticides design using advanced technologies. Springer-Verlag Berlin Heidelberg, Netherlands.CrossRefGoogle Scholar
Isman, M.B., Miresmailli, S., and MacHial, C. 2011. Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochemistry Reviews, 10: 197–204.CrossRefGoogle Scholar
Jaenson, T.G.T., Pålsson, K., and Borg-Karlson, A.-K. 2006. Evaluation of extracts and oils of mosquito (Diptera: Culicidae) repellent plants from Sweden and Guinea-Bissau. Journal of Medical Entomology, 43: 115–119.CrossRefGoogle ScholarPubMed
Judzentiene, A. and Mockute, D. 2010. Essential oil composition of two yarrow taxonomic forms. Central European Journal of Biology, 5: 346–352.Google Scholar
Kotan, R., Cakir, A., Dadasoglu, F., Aydin, T., Cakmakci, R., Ozer, H., et al. 2010. Antibacterial activities of essential oils and extracts of Turkish Achillea, Satureja and Thymus species against plant pathogenic bacteria. Journal of the Science of Food and Agriculture, 90: 145–160.CrossRefGoogle ScholarPubMed
Kraus, B., Koeniger, N., and Fuchs, S. 1994. Screening of substances for their effect on Varroa jacobsoni: attractiveness, repellency, toxicity and masking effects of ethereal oils. Journal of Apicultural Research, 33: 34–43.CrossRefGoogle Scholar
Lakshmi, T., Geetha, R.V., Roy, A., and Aravind Kumar, S. 2011. Yarrow (Achillea millefolium L.) a herbal medicinal plant with broad theraputic use: a review. International Journal of Pharmaceutical Sciences Review and Research, 9: 136–141.Google Scholar
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). Journal of Economic Entomology, 90: 883–892.CrossRefGoogle Scholar
Levin, S., Sela, N., and Chejanovsky, N. 2016. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor . Scientific Reports, 6: 37710.CrossRefGoogle ScholarPubMed
Light, M. 2019. Chemical ecology and biology of Varroa destructor (Anderson and Trueman), a primary pest of western honey bees (Apis mellifera L.) [online]. Acadia University, Wolfville, Nova Scotia, Canada. Available from https://scholar.acadiau.ca/islandora/object/theses:3210 [accessed 24 September 2020].Google Scholar
Lindberg, C.M., Melathopoulos, A.P., and Winston, M.L. 2000. Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymenoptera: Apidae) parasite. Journal of Economic Entomology, 93: 189–198.CrossRefGoogle ScholarPubMed
Maisonnasse, A., Lenoir, J.C., Costagliola, G., Beslay, D., Choteau, F., Crauser, D., et al. 2009. A scientific note on E-β-ocimene, a new volatile primer pheromone that inhibits worker ovary development in honey bees. Apidologie, 40: 562–564.CrossRefGoogle Scholar
Melathopoulos, A.P., Winston, M.L., Whittington, R., Higo, H., and Le Doux, M. 2000. Field evaluation of neem and canola oil for the selective control of the honey bee (Hymenoptera: Apidae) mite parasites Varroa jacobsoni (Acari: Varroidae) and Acarapis woodi (Acari: Tarsonemidae). Journal of Economic Entomology, 93: 559–567.CrossRefGoogle Scholar
Mitich, L.W. 1990. Yarrow: the herb of Achilles. Weed Technology, 4: 451–453.CrossRefGoogle Scholar
Nadim, M.M., Malik, A.A., Ahmad, J., and Bakshi, S.K. 2011. The essential oil composition of Achillea millefolium L. cultivated under tropical condition in India. World Journal of Agricultural Sciences, 7: 561–565.Google Scholar
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. Entomologia Experimentalis et Applicata, 76: 217–222.CrossRefGoogle Scholar
Newcomb, L. 1989. Newcomb’s Wildflower Guide. Little, Brown and Company, New York, New York, United States of America.Google Scholar
Park, I., Lee, S., Choi, D., Park, J., and Ahn, Y. 2003. Insecticidal activities of constituents identified in the essential oil from leaves of Chamaecyparis obtusa against Callosobruchus chinensis (L.) and Sitophilus oryzae (L.). Journal of Stored Products Research, 49: 375–384.CrossRefGoogle Scholar
Peng, G., Kashio, M., Morimoto, T., Li, T., Zhu, J., Tominaga, M., and Kadowaki, T. 2015. Plant-derived tick repellents activate the honey bee ectoparasitic mite TRPA1. Cell Reports, 12: 190–202.CrossRefGoogle ScholarPubMed
Plettner, E., Eliash, N., Singh, N.K., Pinnelli, G.R., and Soroker, V. 2017. The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie, 48: 78–92.CrossRefGoogle Scholar
R Core Team. 2018. R: a language and environment for statistical computing [online]. Foundation for Statistical Computing, Vienna, Austria. Available from https://www.r-project.org/foundation/ [accessed 24 September 2020].Google Scholar
Raguso, R.A. and Pellmyr, O. 1998. Dynamic headspace analysis of floral volatiles: a comparison of methods. Oikos, 81: 238.CrossRefGoogle Scholar
Rahimi, A., Del, Y.K., and Moradpour, F. 2017. The effect of thyme (Thymus caucasicus) ethanol extract on Varroa mite (Varroa destructor), an ectoparasite mite of Apis mellifera meda (Hym: Apidae). Biologija, 63: 177–184.CrossRefGoogle Scholar
Ramsey, S.D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J.D., Cohen, A., et al. 2019. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116: 1792–1801.CrossRefGoogle Scholar
Regnault-Roger, C., Vincent, C., and Arnason, J.T. 2012. Essential oils in insect control: low-risk products in a high-stakes world. Annual Review of Entomology, 57: 405–424.CrossRefGoogle Scholar
Rohloff, J., Skagen, E.B., Steen, A.H., and Iversen, T.H. 2000. Production of yarrow (Achillea millefolium L.) in Norway: essential oil content and quality. Journal of Agricultural and Food Chemistry, 48: 6205–6209.CrossRefGoogle ScholarPubMed
Rosenkranz, P., Aumeier, P., and Ziegelmann, B. 2010. Biology and control of Varroa destructor . Journal of Invertebrate Pathology, 103: S96–S119.CrossRefGoogle ScholarPubMed
Ruffinengo, S., Maggi, M., Faverin, C., García de la Rosa, S.B., Bailac, P., Principal, J., and Eguaras, M. 2007. Essential oils toxicity related to Varroa destructor and Apis mellifera under laboratory conditions. Instituto Nacional de Investigaciones Agrícolas Venezuela, Zootecnia Tropical, 25: 63–69.Google Scholar
Shutler, D. and Campbell, A.A. 2007. Experimental addition of greenery reduces flea loads in nests of a non-greenery using species, the tree swallow Tachycineta bicolor . Journal of Avian Biology, 38: 7–12.CrossRefGoogle Scholar
Singh, N.K., Eliash, N., Kamer, Y., Zaidman, I., Plettner, E., and Soroker, V. 2015. The effect of DEET on chemosensing of the honey bee and its parasite Varroa destructor . Apidologie, 46: 380–391.CrossRefGoogle Scholar
Siramon, P., Ohtani, Y., and Ichiura, H. 2009. Biological performance of Eucalyptus camaldulensis leaf oils from Thailand against the subterranean termite Coptotermes formosanus Shiraki. Journal of Wood Science, 55: 41–46.CrossRefGoogle Scholar
Soroker, V., Singh, N.K., Eliash, N., and Plettner, E. 2019. Olfaction as a target for control of honeybee parasite mite Varroa destructor. In Olfactory concepts of insect control-alternative to insecticides (1st edition). Edited by J.-F. Picimbon. Springer International Publishing, Heidelberg, Germany. Pp. 117–134.Google Scholar
Stanimirović, Z., Glavinić, U., Lakić, N., Radović, D., Ristanić, M., Tarić, E., and Stevanović, J. 2017. Efficacy of plant-derived formulation “argus ras” in Varroa destructor control. Acta Veterinaria, 67: 191–200.CrossRefGoogle Scholar
Stein, S.E., Mikaia, A., White, E., Zaikin, V., Zhu, D., Sparkman, O.D., et al. 2011. NIST standard reference database 1A - user’s guide. Version 2.0. National Institute of Standards and Technology, Gaithersburg, Maryland, United States of America. Pp. 1–65.Google Scholar
Syntech. 2015. Electroantennography: a practical introduction [online]. Syntech Original Research Instruments, Kirchzarten, Germany. Available from: http://www.ockenfels-syntech.com/wp-content/uploads/EAGpract_man_fin [accessed 24 September 2020].Google Scholar
Torto, B., Carroll, M.J., Duehl, A., Fombong, A.T., Gozansky, T.K., Nazzi, F., et al. 2013. Standard methods for chemical ecology research in Apis mellifera . Journal of Apicultural Research, 52: 1–34.Google Scholar
Tutun, H., Koç, N., and Kart, A. 2018. Plant essential oils used against some bee diseases. Turkish Journal of Agriculture - Food Science and Technology, 6: 34.Google Scholar
Von Rudnew, D.F. and Smeljanez, W.P. 1970. Ursachen der Massenvermehru ng einiger Forstschädlingsarten. Anzeiger für Schädlingskunde, 43: 177–184.Google Scholar
Warwick, S.I. and Black, L. 1982. The biology of Canadian weeds. 52. Achillea millefolium L. S.L. Canadian Journal of Plant Science, 62: 163–182.CrossRefGoogle Scholar
Yatagai, M., Makihara, H., and Oba, K. 2002. Volatile components of Japanese cedar cultivars as repellents related to resistance to Cryptomeria bark borer. Journal of Wood Science, 48: 51–55.CrossRefGoogle Scholar
Supplementary material: File

Light et al. Supplementary Materials

Light et al. Supplementary Materials

Download Light et al. Supplementary Materials(File)
File 68.7 KB