Journal of Chemical Ecology

, Volume 44, Issue 6, pp 565–575 | Cite as

Inhibitory Effects of Semiochemicals on the Attraction of an Ambrosia Beetle Euwallacea nr. fornicatus to Quercivorol

  • John A. Byers
  • Yonatan Maoz
  • David Wakarchuk
  • Daniela Fefer
  • Anat Levi−Zada


The Euwallacea fornicatus (Eichhoff) species complex includes the polyphagous shot hole borer (PSHB), an ambrosia beetle infesting avocado limbs, Persea americana Mill. Synthetic quercivorol, a monoterpene alcohol, is known to attract females (males are flightless) over a range of release rates spanning three orders of magnitude. The upper release dose was extended 10-fold using sticky traps baited with quercivorol released at 1× (0.126 mg/day), 10×, and 108× relative rates to obtain a dose−response curve fitting a kinetic formation function. Naturally infested limbs of living avocado trees were wrapped with netting to exclude the possibility of catching emerging beetles on the encircling sticky traps. The results indicate PSHB are significantly attracted to infested limbs. Ethanol released over a 64-fold range (lowest rate of 7.5 mg/day) was moderately inhibitory of PSHB attraction to 1× quercivorol. β-caryophyllene and eucalyptol did not appear to affect attraction at the rates tested. A field test of potential inhibitors of 1× quercivorol was done using ~1 mg/day releases of monoterpene ketones: (−)-(S)-verbenone, (+)-(R)-verbenone, 3-methyl-2-cyclo-hexen-1-one (MCH or seudenone), piperitone, (+)-(S)-carvone, and racemic cryptone. Only piperitone and the two enantiomers of verbenone were strongly inhibitory. A blend of piperitone and verbenone tested together at different distances (0, 0.5, 1, 2, and 4 m) from a 1× quercivorol baited sticky trap became increasingly ineffective in inhibiting the attractant as separation distance increased. Due to the relatively short-range repellency (<1 m), the inhibitors would need to be released from several places on each tree to effectively repel PSHB from avocado trees. Effective attraction radii, EAR, and circular EARc are estimated for the quercivorol baits released at 1×, 10× and 108× rates. Push-pull simulations of moving beetles were performed in 1 ha plots with 2, 4, or 16 traps of 10× EARc and 400 trees (0, 1, or 3 inhibitors per tree) of which ten had an infested limb (EARc = 0.5 m). The simulations indicate that push-pull methods would be more effective in reducing PSHB mating than simply using mass-trapping alone.


Push-pull Repellent Attractant Effective attraction radius Semiochemicals Mass trapping 



We thank Kibbutz Ma’agan Michael avocado growers for assistance in setup and maintenance of field experiments. This research was supported by a grant from the Israel Avocado Growers Association #0390320 of 2017.


  1. Bedard WD, Tilden PE, Wood DL, Lindahl KQ, Rauch PA (1980) Effects of verbenone and trans-verbenol on the response of Dendroctonus brevicomis to natural and synthetic attractant in the field. J Chem Ecol 6:997–1013CrossRefGoogle Scholar
  2. Byers JA (1987) Interactions of pheromone component odor plumes of western pine beetle. J Chem Ecol 13:2143–2157CrossRefPubMedGoogle Scholar
  3. Byers JA (1988) Novel diffusion-dilution method for release of semiochemicals: Testing pheromone component ratios on western pine beetle. J Chem Ecol 14:199–212CrossRefPubMedGoogle Scholar
  4. Byers JA (1989) Chemical ecology of bark beetles. Experientia 45:271–283CrossRefGoogle Scholar
  5. Byers JA (1992) Attraction of bark beetles, Tomicus piniperda, Hylurgops palliatus, and Trypodendron domesticum and other insects to short-chain alcohols and monoterpenes. J Chem Ecol 18:2385–2402CrossRefPubMedGoogle Scholar
  6. Byers JA (2004) Chemical ecology of bark beetles in a complex olfactory landscape. In: Lieutier F, Day KR, Battisti A, Grégoire JC, Evans H (eds) Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Kluwer Academic Publishers, Dordrecht, pp 89–134CrossRefGoogle Scholar
  7. Byers JA (2011) Analysis of vertical distributions and effective flight layers of insects: Three-dimensional simulation of flying insects and catch at trap heights. Environ Entomol 40:1210–1222CrossRefPubMedGoogle Scholar
  8. Byers JA (2012a) Estimating insect flight densities from attractive trap catches and flight height distributions. J Chem Ecol 38:592–601CrossRefPubMedGoogle Scholar
  9. Byers JA (2012b) Modelling female mating success during mass trapping and natural competitive attraction of searching males or females. Entomol Exp Appl 145:228–237CrossRefGoogle Scholar
  10. Byers JA (2013) Modeling and regression analysis of semiochemical dose−response curves of insect antennal reception and behavior. J Chem Ecol 39:1081–1089CrossRefPubMedGoogle Scholar
  11. Byers JA, Naranjo SE (2014) Detection and monitoring of pink bollworm moths and invasive insects using pheromone traps and encounter rate models. J Appl Ecol 51:1041–1049CrossRefGoogle Scholar
  12. Byers JA, Wood DL (1980) Interspecific inhibition of the response of the bark beetles, Dendroctonus brevicomis and Ips paraconfusus, to their pheromones in the field. J Chem Ecol 6:149–164CrossRefGoogle Scholar
  13. Byers JA, Lanne BS, Löfqvist J (1989) Host-tree unsuitability recognized by pine shoot beetles in flight. Experientia 45:489–492CrossRefGoogle Scholar
  14. Byers JA, Zhang QH, Birgersson G (2004) Avoidance of nonhost plants by a bark beetle, Pityogenes bidentatus, in a forest of odors. Naturwissenschaften 91:215–219CrossRefPubMedGoogle Scholar
  15. Byers JA, Maoz Y, Levi-Zada A (2017) Attraction of the Euwallacea sp. near fornicatus (Coleoptera: Curculionidae) to quercivorol and to infestations in avocado. J Econ Entomol 110:1512–1517CrossRefPubMedGoogle Scholar
  16. Calnaido D (1965) The flight and dispersal of shot-hole borer of tea (Xyleborus fornicatus Eichh., Coleoptera: Scolytidae). Entomol Exp Appl 8:249–262CrossRefGoogle Scholar
  17. Carrillo D, Narvaez T, Cossé AA, Stouthamer R, Cooperband M (2015) Attraction of Euwallacea nr. fornicatus (Coleoptera: Curculionidae: Scolytinae) to lures containing quercivorol. Fla Entomol 98:780–782CrossRefGoogle Scholar
  18. Carrillo D, Cruz LF, Kendra PE, Narvaez TI, Montgomery WS, Monterroso A, De Grave C, Cooperband MF (2016) Distribution, pest status and fungal associates of Euwallacea nr. fornicatus in Florida avocado groves. Insects 7:55, 11 p. CrossRefPubMedCentralGoogle Scholar
  19. Cook SM, Khan ZR, Pickett JA (2007) The use of pushpull strategies in integrated pest management. Annu Rev Entomol 52:375–400CrossRefPubMedGoogle Scholar
  20. Cooperband MF, Stouthamer R, Carrillo D, Eskalen A, Thibault T, Cossé AA, Castrillo LA, Vandenberg JD, Rugman-Jones PF (2016) Biology of two members of the Euwallacea fornicatus species complex (Coleoptera: Curculionidae: Scolytinae), recently invasive in the U.S.A., reared on an ambrosia beetle artificial diet. Agric For Entomol 18:223–237CrossRefGoogle Scholar
  21. Eskalen A, Gonzalez A, Wang DH, Twizeyimana M, Mayorquin JS (2012) First report of a Fusarium sp. and its vector tea shot hole borer (Euwallacea nr. fornicatus) causing Fusarium dieback on avocado in California. Plant Dis 96:1070CrossRefGoogle Scholar
  22. Eskalen A, Stouthamer R, Lynch SC, Rugman-Jones PF, Twizeyimana M, Gonzalez A, Thibault T (2013) Host range of Fusarium dieback and its ambrosia beetle (Coleoptera: Scolytinae) vector in southern California. Plant Dis 97:938–951CrossRefGoogle Scholar
  23. Forsse E, Solbreck CH (1985) Migration in the bark beetle Ips typographus L.: Duration, timing and height of flight. Z Angew Entomol 100:47–57CrossRefGoogle Scholar
  24. Freeman S, Protasov A, Sharon M, Mohotti K, Eliyahu M, Okon-Levy N, Maymon M, Mendel Z (2012) Obligate feed requirement of Fusarium sp. nov., an avocado wilting agent, by the ambrosia beetle Euwallacea aff. fornicata. Symbiosis 58:245–251CrossRefGoogle Scholar
  25. Furniss MM, Kline LN, Schmitz RF, Rudinsky JA (1972) Tests of three pheromones to induce or disrupt aggregation of Douglas-fir beetles (Coleoptera: Scolytidae) on live trees. Ann Entomol Soc Am 65:1227–1232CrossRefGoogle Scholar
  26. Furniss MM, Baker BH, Hostetler BB (1976) Aggregation of spruce beetles (Coleoptera) to seudenol and repression of attraction by methylcyclohexenone in Alaska. Can Entomol 108:1297–1302CrossRefGoogle Scholar
  27. Gillette NE, Mehmel CJ, Mori SR, Webster JN, Wood DL, Erbilgin N, Owen DR (2012) The push–pull tactic for mitigation of mountain pine beetle (Coleoptera: Curculionidae) damage in lodgepole and whitebark pines. Environ Entomol 41:1575–1586CrossRefPubMedGoogle Scholar
  28. Hanula JL, Sullivan B (2008) Manuka oil and phoebe oil are attractive baits for Xyleborus glabratus (Coleoptera Scolytinae), the vector of laurel wilt. Environ Entomol 37:1403–1409CrossRefPubMedGoogle Scholar
  29. Hughes MA, Martini X, Kuhns E, Colee J, Mafra-Neto A, Stelinski LL, Smith JA (2017) Evaluation of repellents for the redbay ambrosia beetle, Xyleborus glabratus, vector of the laurel wilt pathogen. J Appl Entomol.
  30. Hulcr J, Stelinski LL (2017) The ambrosia symbiosis: From evolutionary ecology to practical management. Annu Rev Entomol 62:285–303CrossRefPubMedGoogle Scholar
  31. Jactel H, Gaillard J (1991) A preliminary study of the dispersal potential of Ips sexdentatus Boern (Coleoptera: Scolytidae) with an automatically recording flight mill. J Appl Entomol 112:138–145CrossRefGoogle Scholar
  32. Kendra PE, Montgomery WS, Niogret J, Peña JE, Capinera JL, Brar G, Epsky ND, Heath RR (2011) Attraction of the redbay ambrosia beetle, Xyleborus glabratus, to avocado, lychee, and essential oil lures. J Chem Ecol 37:932–942CrossRefPubMedGoogle Scholar
  33. Kendra PE, Niogret J, Montgomery WS, Sanchez JS, Deyrup MA, Pruett GE, Ploetz RC, Epsky ND, Heath RR (2012) Temporal analysis of sesquiterpene emissions from manuka and phoebe oil lures and efficacy for attraction of Xyleborus glabratus (Coleoptera: Curculionidae: Scolytinae). J Econ Entomol 105:659–669CrossRefPubMedGoogle Scholar
  34. Kendra PE, Montgomery WS, Niogret J, Pruett GE, Mayfield AE III, MacKenzie M, Deyrup MA, Bauchan GR, Ploetz RC, Epsky ND (2014) North American Lauraceae: Terpenoid emissions, relative attraction and boring preferences of redbay ambrosia beetle, Xyleborus glabratus (Coleoptera: Curculionidae: Scolytinae). PLoS One 9:e102086CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kendra PE, Owens D, Montgomery WS, Narvaez TI, Bauchan GR, Schnell EQ, Tabanca N, Carrillo D (2017) α-Copaene is an attractant, synergistic with quercivorol, for improved detection of Euwallaceanr. fornicatus (Coleoptera: Curculionidae:Scolytinae). PLoS One 12:e0179416CrossRefPubMedPubMedCentralGoogle Scholar
  36. Klimetzek D, Köhler J, Vité JP (1986) Dosage response to ethanol mediates host selection by “secondary” bark beetles. Naturwissenschafren 73:270–272CrossRefGoogle Scholar
  37. Kuhns EH, Martini X, Tribuiani Y, Coy M, Gibbard C, Peña J, Hulcr J, Stelinski LL (2014) Eucalyptol is an attractant of the redbay ambrosia beetle, Xyleborus glabratus. J Chem Ecol 40:355–362CrossRefPubMedGoogle Scholar
  38. Levi-Zada A, Sadowsky A, Dobrinin S, Ticuchinski T, David M, Fefer D, Dunkelblum E, Byers JA (2017) Monitoring and mass-trapping methodologies using pheromones: the lesser date moth Batrachedra amydraula. Bull Entomol Res 108:58–68CrossRefPubMedGoogle Scholar
  39. Lynch SC, Twizeyimana M, Mayorquin JS, Wang DH, Na F, Kayim M, Kasson MT, Thu PQ, Bateman C, Rugman-Jones P, Hulcr J, Stouthamer R, Eskalen A (2016) Identification, pathogenicity and abundance of Paracremonium pembeum sp. nov. and Graphium euwallaceae sp. nov. − two newly discovered mycangial associates of the polyphagous shot hole borer (Euwallacea sp.) in California. Mycologia 108:313–329CrossRefPubMedGoogle Scholar
  40. Mendel Z, Protasov A, Sharon M, Zveibil A, Yehuda SB, O’Donnell K, Rabaglia R, Wysoki M, Freeman S (2012) An Asian ambrosia beetle Euwallacea nr. fornicatus and its novel symbiotic fungus Fusarium sp. pose a serious threat to the Israeli avocado industry. Phytoparasitica 40:235–238CrossRefGoogle Scholar
  41. Miller JR, Cowles RS (1990) Stimulo-deterrent diversion: a concept and its possible application to onion maggot control. J Chem Ecol 16:3197–3212Google Scholar
  42. O’Donnell K, Sink S, Libeskind-Hadas R, Hulcr J, Kasson MR, Ploetz RC, Konkol JL, Ploetz JN, Carrillo D, Campbell A, Duncan RE, Liyanage PNH, Eskalen A, Na F, Geiser DM, Bateman C, Freeman S, Mendel Z, Sharon M, Aoki T, Cossé AA, Rooney AP (2015) Discordant phylogenies suggest repeated host shifts in the Fusarium–Euwallacea ambrosia beetle mutualism. Fungal Genet Biol 82:277–290CrossRefPubMedGoogle Scholar
  43. Paine TD, Birch MC, Miller JC (1984) Use of pheromone traps to suppress populations of Scolytus multistriatus (Marsham) (Coleoptera: Scolytidae) in three isolated communities of elms. Agric Ecosyst Environ 11:309–318CrossRefGoogle Scholar
  44. Pyke B, Rice M, Sabine B, Zalucki MP (1987) The push-pull strategy – behavioural control of Heliothis. Aust Cottongrower 7:9Google Scholar
  45. Rudinsky JA, Kline LN, Diekman JD (1975) Response–inhibition by four analogues of MCH, an antiggregative pheromone of the Douglas-fir beetle. J Econ Entomol 68:527–528CrossRefGoogle Scholar
  46. Schroeder LM, Lindelöw Å (1989) Attraction of scolytids and associated beetles by different absolute amounts and proportions of α-pinene and ethanol. J Chem Ecol 15:807–817CrossRefPubMedGoogle Scholar
  47. Stouthamer R, Rugman-Jones P, Thu PQ, Eskalen A, Thibault T, Hulcr J, Wang LJ, Jordal BH, Chen CY, Cooperband M, Lin CS, Kamata N, Lu SS, Masuya H, Mendel Z, Rabaglia R, Sanguansub S, Shih HH, Sittichaya W, Zong S (2017) Tracing the origin of a cryptic invader: phylogeography of the Euwallacea fornicatus (Coleoptera: Curculionidae: Scolytinae) species complex. Agric For Entomol.
  48. Thomas AF, Willhalm B, Bowie JH (1967) Mass spectra and organic synthesis. Part VIII. The mass spectra of piperitone, the piperitols, and related products. J Chem Soc B 392–400.
  49. Tokoro M, Kobayashi M, Saito S, Kinuura H, Nakashima T, Shoda-Kagaya E, Kashiwagi T, Tebayashi S, Kim C, Mori K (2007) Novel aggregation pheromone, (1S,4R)-p-menth-2-en-1-ol, of the ambrosia beetle, Platypus quercivorus (Coleoptera: Platypodidae). Bull For For Prod Res Inst 6:49–57Google Scholar
  50. Turek C, Stintzing FC (2013) Stability of essential oils: A review. Compr Rev Food Sci Food Saf 12(1):40–53CrossRefGoogle Scholar
  51. Wood SL (1982) The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Naturalist Memoirs 6:l–1359Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • John A. Byers
    • 1
  • Yonatan Maoz
    • 2
  • David Wakarchuk
    • 3
  • Daniela Fefer
    • 4
  • Anat Levi−Zada
    • 4
  1. 1.Department of Entomology, Robert H. Smith Faculty of Agriculture, Food and EnvironmentThe Hebrew University of JerusalemRehovotIsrael
  2. 2.The Israel Fruit Growers AssociationYahudIsrael
  3. 3.Synergy SemiochemicalsBurnabyCanada
  4. 4.Institute of Plant Protection, Agricultural Research Organization, Volcani CenterRishon LeZionIsrael

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