Eur. J. Entomol. 107 (4): 541-548, 2010 | DOI: 10.14411/eje.2010.062

Identification of limonene as a potential kairomone of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae)

Ammar ALHMEDI, Eric HAUBRUGE, Frédéric FRANCIS
Department of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés 2,

Chemical cues involved in both host location and oviposition by Harmonia axyridis Pallas (Coleoptera: Coccinellidae) were investigated in laboratory and field experiments. Among the five volatiles tested in a four-arm olfactometer ((E)-β-farnesene, β-pinene, β-caryophyllene, cis-3-hexen-1-ol, and limonene), gravid H. axyridis females were significantly attracted to limonene and β-caryophyllene. These two chemicals also increased H. axyridis oviposition on plants. Attraction of H. axyridis towards limonene was further tested under field conditions using controlled-release dispensers. (E)-β-farnesene, a major aphid alarm pheromone and a potential predator kaironome, was also tested in this study. Field data confirmed those from laboratory studies concerning the attraction of H. axyridis towards limonene and a lack of response to (E)-β-farnesene. In contrast, the aphid predator Episyrphus balteatus DeGeer (Diptera: Syrphidae) was attracted to (E)-β-farnesene but not to limonene. These findings indicate that H. axyridis uses chemicals, such as limonene, for prey location and oviposition, and support the potential use of volatiles in the management of H. axyridis.

Keywords: Coccinellidae, Harmonia axyridis, four-arm olfactometer, host location, induced semiochemical, limonene, b-caryophyllene, natural enemies, oviposition stimulant, pest management

Received: March 17, 2010; Revised: May 17, 2010; Accepted: May 17, 2010; Published: October 20, 2010  Show citation

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ALHMEDI, A., HAUBRUGE, E., & FRANCIS, F. (2010). Identification of limonene as a potential kairomone of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae). EJE, 107(4), 541-548. doi: 10.14411/eje.2010.062
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    References

    1. ADRIAENS T., BRANQUART E. & MAES D. 2003: The multicoloured Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belg. J. Zool. 133: 195-196
    2. ADRIAENS T., SAN MARTIN Y GOMEZ G. & MAES D. 2008: Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl 53: 69-88 Go to original source...
    3. AL ABASSI S.A., BIRKETT M.A., PETTERSSON J., PICKETT J.A., WADHAMS L.J. & WOODCOCK C.M. 2000: Response of the seven-spot ladybird to an alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J. Chem. Ecol. 26: 1765-1771 Go to original source...
    4. ALHMEDI A., HAUBRUGE E., BODSON B. & FRANCIS F. 2007: Aphidophagous guilds on nettle (Urtica dioica) strips close to fields of green pea, rape and wheat. Insect Sci. 14: 419-424 Go to original source...
    5. ALYOKHIN A. & SEWELL G. 2004: Changes in a lady beetle community following the establishment of three alien species. Biol. Invasions 6: 463-471 Go to original source...
    6. BHASIN A., MORDUE A.J. & MORDUE W. 2000: Electrophysiological and behavioral identification of host kairomones as olfactory cues for Culicoides impuntatus and C. nubeculosis. Physiol. Entomol. 25: 6-16 Go to original source...
    7. BOO K.S., CHUNG I.B., HAN K.S., PICKETT J.A. & WADHAMS L.J. 1998: Response of the lacewing Chrysopa cognata to pheromones of its aphid prey. J. Chem. Ecol. 24: 631-639 Go to original source...
    8. BOTTRELL D.G. & BARBOSA P. 1998: Manipulating natural enemies by plant variety selection and modification: A realistic strategy? Annu. Rev. Entomol. 43: 347-367 Go to original source...
    9. BROWN M.W. 2004: Role of the aphid predator guild in controlling spirea aphid populations on apple in West Virginia, USA. Biol. Control 29: 189-198 Go to original source...
    10. BROWN A.E., RIDDICK E.W., ALDRICH J.R. & HOLMES W.E. 2006: Identification of (-)-E-caryophyllene as a gender-specific terpene produced by the multicolored Asian lady beetle. J. Chem. Ecol. 32: 2489-2499 Go to original source...
    11. BURNS D.A., MCDONNELL J.J., HEMPTINNE J.-L., LOGNAY G. & DIXON A.F.G. 1998: Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. J. Insect Physiol. 44: 1163-1171 Go to original source...
    12. CAMPBELL C.A.M., PETTERSSON J., PICKETT J.A., WADHAMS L.J. & WOODCOCK C.M. 1993: Spring migration of damson hop aphid, Phorodon humuli (Homoptera, Aphididae), and summer host plant derived semiochemicals released on feeding. J. Chem. Ecol. 19: 1569-1576 Go to original source...
    13. CARDE R.T. 1996: Odour plumes and odour-mediated flight in insects. In Bock G.R. & Cardew G. (eds): Olfaction in Mosquito-host Interactions. Ciba Foundation Symposium 200, John Wiley & Sons, Chichester, pp. 54-70 Go to original source...
    14. COLAZZA S., FUCARINO A., PERI E., SALERMO G., CONTI E. & BIN F. 2001: Cues mediating host location in Trissolcus basalts: The role of volatiles induced by host eggs-plant interaction. In Proceedings of the 18th Annual Meeting of the International Society of Chemical Ecology , Lake Tahoe, 81 pp
    15. COOK S.M., KHAN Z.R. & PICKETT J.A. 2007: The use of pushpull strategies in integrated pest management. Annu. Rev. Entomol. 52: 375-400 Go to original source...
    16. DAWSON G.W., GRIFFITHS D.C., PICKETT J.A., SMITH M.C. & WOODCOCK C.M. 1984: Natural inhibition of aphid alarm pheromone. Entomol. Exp. Appl. 36: 197-199 Go to original source...
    17. DE BOER J.G., POSTHUMS M.A. & DICKE M. 2004: Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J. Chem. Ecol. 30: 2215-2230 Go to original source...
    18. DE BOER J.G., SNOEREN T.A.L. & DICKE M. 2005: Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim. Behav. 69: 869-879 Go to original source...
    19. DICKE M., SABELIS M.W., TAKABAYASHI J., BRUIN J. & POSTHUMS M.A. 1990: Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol. 16: 3091-3118 Go to original source...
    20. ELKINTON J.S., SCHAL C., ONO T. & CARDE R.T. 1987: Pheromone puff trajectory and upwind flight of male gypsy moths in a forest. Physiol. Entomol. 12: 399-406 Go to original source...
    21. FLINT H.M., SALTER S.S. & WALTERS S. 1979: Caryophyllene: An attractant for the green lacewing. Environ. Entomol. 8: 1123-1125 Go to original source...
    22. FRANCIS F., LOGNAY G. & HAUBRUGE E. 2004: Olfactory responses to aphid and host plant volatile releases: E-Efarnesene an effective kairomone for the predator Adalia bipunctata. J. Chem. Ecol. 30: 741-755 Go to original source...
    23. FRANCIS F., MARTIN T., LUCAS G. & HAUBRUGE E. 2005a: Role of (E)-E-farnesene in systematic aphid prey location by Episyrphus balteatus larvae (Diptera: Syrphidae). Eur. J. Entomol. 102: 431-436 Go to original source...
    24. FRANCIS F., VANDERMOTEN S., VERHEGGEN F., LOGNAY G. & HAUBRUGE E. 2005b: Is the (E)-E-Farnesene only volatile terpenoid in aphids? J. Appl. Entomol. 129: 6-11 Go to original source...
    25. GOUINGUENE S., PICKETT J.A., WADHAMS L.J., BIRKETT M.A. & TURLINGS T.C.J. 2005: Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol. 31: 1023-1038 Go to original source...
    26. HEIDARI M. & COPLAND M.J.W. 1992: Host finding by Cryptolaemus montrouzieri (Col., Coccinellidae) a predator of mealybugs (Hom. Pseudococcidae). Entomophaga 37: 621-625 Go to original source...
    27. HEMPTINNE J.L., GAUDIN M., DIXON A.F.G. & LOGNAY G. 2000: Social feeding in ladybird beetles: adaptive significance and mechanism. Chemoecology 10: 149-152 Go to original source...
    28. HEMPTINNE J.-L., LOGNAY G., DOUMBIA M. & DIXON A.F.G. 2004: Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the larvae of the two spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11: 43-47 Go to original source...
    29. HODEK I. & HONEK A. 1996: Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, 464 pp Go to original source...
    30. HUELSMAN M.F. & KOVACH J. 2004: Behavior and treatment of the multicolored Asian lady beetle (Harmonia axyridis) in urban environments. Am. Entomol. 50: 163-164 Go to original source...
    31. HULCR J., UBIK K. & VRKOC J. 2006: The role of semiochemicals in tritrophic interactions between the spruce bark beetle Ips typographus, its predators and infested spruce. J. Appl. Entomol. 130: 275-283 Go to original source...
    32. HUNTER M.D. 2002: A breath of fresh air: Beyond laboratory studies of plant volatile-natural enemy interactions. Agr. Forest Entomol. 4: 81-86 Go to original source...
    33. JAMES D.G. 2003a: Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: Methyl salicylate and the green lacewing, Chrysopa nigricornis. J. Chem. Ecol. 29: 1601-1609. Go to original source...
    34. JAMES D.G. 2003b: Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ. Entomol. 32: 977-982 Go to original source...
    35. JAMES D.G. & PRICE S.T. 2004: Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J. Chem. Ecol. 30: 1613-1628 Go to original source...
    36. JAMES D.G., PRICE T.S. & WRIGHT L.C. 2003: Mites and aphids in Washington hops: Candidates for augmentative or conservation biological control. In: Proceeding of 1st International Symposium Biological Control of Arthropods. USDA Forest Service Pub. FHTET-03-05, pp. 189-195
    37. JOHNE B., SPRAUER S., WEISSBECKER B. & SCHUTZ S. 2006: Influence of flower odor compounds on oviposition of the horse chestnut leaf miner Cameraria ohridella (Deschka and Dimic). Mitt. Dt. Ges. Allg. Angew. Entomol. 14: 355-360
    38. KALASKAR A. & EVANS E.W. 2001: Larval responses of aphidophagous lady beetles (Coleoptera: Coccinellidae) to weevil larvae versus aphid as prey. Ann. Entomol. Soc. Am. 94: 76-81 Go to original source...
    39. KESSLER A. & BALDWIN I.T. 2001: Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144 Go to original source...
    40. KOCH R.L., VENETTE R.C. & HUTCHINSON W.D. 2005: Influence of alternate prey on predation of monarch butterfly (Lepidoptera: Nymphalidae) larvae by the multicoloured Asian lady beetle (Coleoptera: Coccinellidae). Environ. Entomol. 34: 410-416 Go to original source...
    41. KUZNETSOV V.N. 1997: Lady Beetles of the Russian Far East. The Sandhill Crane Press, Gainesville, 248 pp
    42. LEWIS W.J., JONES R.L., NORDLUND D.A., GUELDNER R.C., TEAL P.E.A. & TUMLINSON J.H. 1982: Kairomones and their use for management of entomophagous insects. XIII. Kairomonal activity for Trichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend of Heliothis zea (Boddie) moths. J. Chem. Ecol. 8: 1323-1331 Go to original source...
    43. LUCAS E., CODERRE D. & VINCENT C. 1997: Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae. Entomol. Exp. Appl. 85: 151-159 Go to original source...
    44. LUCAS E., LABRIE G., VINCENT C. & KOVACH J. 2007: The multicolored Asian ladybeetle, Harmonia axyridis - beneficial or nuisance organism? In Vincent C., Goettel M. & Lazarovitz G. (eds): Biological Control: A Global Perspective. Case Histories from around the World. CABI Publishing, Wallingford, pp. 38-52 Go to original source...
    45. MAJERUS M.E.N. 1994: Ladybirds. New Naturalist series 81, Harper Collins, London, 368 pp
    46. MAJERUS M.E.N., STRAWSON V. & ROY H.E. 2006: The potential impacts of the arrival of the Harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), in Britain. Ecol. Entomol. 31: 207-215 Go to original source...
    47. MCCLURE M.S. 1986: Role of predators in regulation of endemic populations of Matsucoccus matsumurae Kuwana (Homoptera: Margarodidae) in Japan. Environ. Entomol. 15: 976-983 Go to original source...
    48. MICHAUD J.P. 2002: Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ. Entomol. 31: 827-835 Go to original source...
    49. MICHAUD J.P. 2004: Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biol. Control 29: 260-269 Go to original source...
    50. MIZELL R.F.I.I.I., FRAZIER J.L. & NEBEKER T.E. 1984: Response of the clerid predator Thanasimus dubius (F.) to bark beetle pheromones and tree volatiles in a wind tunnel. J. Chem. Ecol. 10: 177-187 Go to original source...
    51. MONDOR E. & ROITBERG B. 2000: Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior? J. Insect Behav. 3: 321-329 Go to original source...
    52. MORAES C.M.D., LEWIS W.J., PARE P.W., ALBORN H.T. & TUMLINSON J.H. 1998: Herbivore-infested plants selectively attract parasitoids. Nature 393: 570-573 Go to original source...
    53. MORAES C.M.D., MESCHER M.C. & TUMLINSON J.H. 2001: Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410: 577-580 Go to original source...
    54. NAKAMUTA K. 1991: Aphid alarm pheromone component, (E)-beta-farnesene, and local search by a predatory lady beetle, Coccinella septempunctata Bruckii mulsant (Coleoptera: Coccinellidae). Appl. Entomol. Zool. 26: 1-7 Go to original source...
    55. NALEPA C.A., KIDD K.A. & AHLSTROM K.R. 1996: Biology of Harmonia axyridis (Coleoptera: Coccinellidae) in winter aggregations. Ann. Entomol. Soc. Am. 89: 681-685 Go to original source...
    56. NALEPA C.A., KENNEDY G.C. & BROWNIE C. 2004: Orientation of multicoloured Asian lady beetles to buildings. Am. Entomol. 50: 165-166
    57. NAULT L.R., EDWARDS L.J. & STYER W.E. 1973: Aphid alarm pheromones: Secretion and reception. Environ. Entomol. 2: 101-105 Go to original source...
    58. NINKOVIC V., AL ABASSI S. & PETTERSSON J. 2001: The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biol. Control 21: 191-195 Go to original source...
    59. PELL J.K. 2008: Ecological approaches to pest management using entomopathogenic fungi; concepts, theory, practice and opportunities. In Ekeski S. & Maniania N.K. (eds): Use of Entomopathogenic Fungi in Biological Pest Management. Research Signpost, Trivandrum, Kerala, pp. 145-178
    60. PETTERSSON J. 1970: Studies on Rhopalosiphum padi (L.) I. Laboratory studies of olfactometric responses to the winter host Prunus padus (L.). LantbrukshGgsk. Ann. 36: 381-399
    61. PETTERSSON J., NINKOVIC V., GLINWOOD R., BIRKETT M.A. & PICKETT J.A. 2005: Foraging in a complex environmentsemiochemicals support searching behaviour of the seven spot ladybird. Eur. J. Entomol. 102: 365-370 Go to original source...
    62. PICKETT J.A. & GRIFFITH D.C. 1980: Composition of aphid alarm pheromones. J. Chem. Ecol. 6: 349-360 Go to original source...
    63. PICKETT J.A., POWELL W., WADHAMS L.J., WOODCOCK C.M. & WRIGHT A.F. 1991: Biochemical interactions between plantherbivore-parasitoid. Proceedings of the 4th European Workshop on Insect Parasitoids, Perugia, Italy . pp. 1-14
    64. PONSONBY D.J. & COPLAND M.J.W. 1995: Olfactory responses by the scale insect predator Chilocorus nigritus F. (Coleoptera: Coccinellidae). Biocontr. Sci. Technol. 5: 83-93 Go to original source...
    65. ROY H.E., BROWN P. & MAJERUS M.E.N. 2006: Harmonia axyridis: a successful biocontrol agent or an invasive threat? In: Eilenberg J. & Hokkanen H. (eds): An Ecological and Societal Approach to Biological Control. Springer, Dordrecht, pp. 295-309 Go to original source...
    66. SCHLYTER F., BIRGERSSON G. & LEUFVEN A. 1989: Inhibition of the attraction to the aggregation pheromone by verbenone and ipsenol: density regulation mechanisms in bark beetle Ips typographus. J. Chem. Ecol. 15: 2263-2277 Go to original source...
    67. SCUTAREANU P., DRUKKER B., BRUIN J., POSTHUMS M.A. & SABELIS M.W. 1997: Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J. Chem. Ecol. 23: 2241-2260 Go to original source...
    68. SHIMODA T., OZAWA R., SANO K., YANO E. & TAKABAYASHI J. 2005: The involvement of volatile infochemicals from spider mites and from food-plants in prey location of the generalist predatory mite: Neoseiulus californicus. J. Chem. Ecol. 31: 2019-2032 Go to original source...
    69. SHU S., GRANT G.G., LANGEVIN D., LOMBARDO D.A. & MACDONALD L. 1997: Oviposition and electroantennogram responses of Dioryctria abietivorella (Lepidoptera: Pyralidae) elicited by monoterpenes and enantiomers from eastern white pine. J. Chem. Ecol. 23: 35-50 Go to original source...
    70. SNYDER W.E. & CLEVENGER G.M. 2004: Negative dietary effects of Colorado potato beetle eggs for the larvae of native and introduced ladybird beetles. Biol. Contr. 31: 353-361 Go to original source...
    71. STANTON M.L. 1983: Spatial patterns in the plant community and their effects upon insect search. In Ahmad S. (ed.): Herbivorous Insects: Host-seeking Behavior and Mechanisms. Academic Press, New York, pp. 125-157 Go to original source...
    72. STUART R.J., MICHAUD J.P., OLSEN L.E. & MCCOY C.W. 2002: Lady beetles as potential predators of the root weevil Diaprepes abbreviatus (Coleoptera: Curculionidae) in Florida citrus. Fla Entomol. 85: 409-416 Go to original source...
    73. TAKABAYASHI J. & DICKE M. 1996: Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1: 109-113 Go to original source...
    74. THALER J.S. 1999: Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 339: 686-688 Go to original source...
    75. THALER J.S. 2002: Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J. Anim. Ecol. 71: 141-150 Go to original source...
    76. TURLINGS T.C.J., LOUGHRIN J.H., MCCALL P.J., OSE U.S.R., LEWIS W.J. & TUMLINSON J.H. 1995: How caterpillar damaged plants protect themselves by attracting parasitic wasps. Proc. Nat. Acad. Sci. USA 92: 4169-4174 Go to original source...
    77. VAN WIJK M., DE BRUIJN J.A.P. & SABELIS W.M. 2008: Predatory mite attraction to herbivore-induced plant odors is not a consequence of attraction to individual herbivore-induced plant volatiles. J. Chem. Ecol. 34: 791-803 Go to original source...
    78. VERHEGGEN F.J., FAGEL Q., HEUSKIN S., LOGNAY G., FRANCIS F. & HAUBRUGE E. 2007: Electrophysiological and behavioral responses of the multicolored asian lady beetle, Harmonia axyridis Pallas, to sesquiterpene semiochemicals. J. Chem. Ecol. 33: 2148-2155 Go to original source...
    79. VERHEGGEN F.J., ARNAUD L., BARTRAM S., GOHY M. & HAUBRUGE E. 2008: Aphid and plant secondary metabolites induce oviposition in an aphidophagous hoverfly. J. Chem. Ecol. 34: 301-307 Go to original source...
    80. VET L.E.M., VAN LENTEREN J.C., HEYMANS M. & MEELIS E. 1983: An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol. Entomol. 8: 97-106 Go to original source...
    81. WEI J.R., YANG Z.Q., HAO H.L. & DU J.W. 2008: (R)-(+)-limonene, kairomone for Dastarcus helophoroides, a natural enemy of longhorned beetles. Agr. Forest Entomol. 10: 323-330 Go to original source...
    82. ZHU J., COSSE A.A., OBRYCKI J.J., BOO K.S. & BAKER T.C. 1999: Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata and the green lacewing, Chrysoperla carnea to semiochemicals released from their prey and host plant: electroantennogram and behavioural responses. J. Chem. Ecol. 25: 1165-1177 Go to original source...

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