Specificity and sensitivity of plant odor-detecting olfactory sensory neurons in Ctenarytaina eucalypti (Sternorrhyncha: Psyllidae)

Journal of Insect Physiology

Volumn 59, Issue 5, 2013, Pages 542-551

  Yuvaraj, Jothi Kumar ^a   Andersson, Martin N ^a   Steinbauer, Martin J ^b   Farnier, Kevin ^b   Anderbrant, Olle ^a  

^a LUND UNIVERSITY   (Sweden)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Ctenarytaina eucalypti; Headspace volatiles; Host finding; Olfactory sensory neuron; Single sensillum recordings

Indexed keywords

VOLATILE ORGANIC COMPOUND;

AMPLITUDE; DOSE-RESPONSE RELATIONSHIP; EVERGREEN TREE; INSECT; ODOR; OLFACTORY CUE; PLANTATION; SENSITIVITY ANALYSIS; VOLATILE SUBSTANCE;

ANIMAL; ARTICLE; CHEMISTRY; EUCALYPTUS; FEMALE; HEMIPTERA; HOST RANGE; MALE; ODOR; OLFACTORY RECEPTOR; PHYSIOLOGY; SENSILLUM; SENSITIVITY AND SPECIFICITY;

ANIMALS; EUCALYPTUS; FEMALE; HEMIPTERA; HOST SPECIFICITY; MALE; ODORS; OLFACTORY RECEPTOR NEURONS; SENSILLA; SENSITIVITY AND SPECIFICITY; SMELL; VOLATILE ORGANIC COMPOUNDS;

CTENARYTAINA EUCALYPTI; EUCALYPTUS; EUCALYPTUS CORDATA; EUCALYPTUS GLOBULUS; PSYLLIDAE; STERNORRHYNCHA; SYMPHYOMYRTUS;

EID: 84876363480     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2013.03.004     Document Type: Article

References (86)

1. Abdelgaleil S.A.M., Mohamed M.I.E., Badawy M.E.I., El-arami S.A.A. Fumigant and contact toxicities of monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase activity. Journal of Chemical Ecology 2009, 35:518-525.
2. Almaas T.J., Christensen T.A., Mustaparta H. Encoding of different features of an olfactory stimulus by the sex pheromone receptors in Heliothis zea. Journal of Comparative Physiology A 1991, 169:249-258.
3. Andersson M.N., Larsson M.C., Schlyter F. Specificity and redundancy in the olfactory system of the bark beetle Ips typographus: single-cell responses to ecologically relevant odors. Journal of Insect Physiology 2009, 55:556-567.
4. Andersson M.N., Larsson M.C., Blaženec M., Jakuš R., Zhang Q.-H., Schlyter F. Peripheral modulation of pheromone response by inhibitory host compound in a beetle. Journal of Experimental Biology 2010, 213:3332-3339.
5. Andersson M.N., Larsson M.C., Svensson G.P., Birgersson G., Rundlöf M., Lundin O., Lankinen Å., Anderbrant O. Characterization of olfactory sensory neurons in the white clover seed weevil, Apion fulvipes (Coleoptera: Apionidae). Journal of Insect Physiology 2012, 58:1325-1333.
6. Andersson M.N., Schlyter F., Hill S.R., Dekker T. What reaches the antenna? How to calibrate odor flux and ligand-receptor affinities. Chemical Senses 2012, 37:403-420.
7. Barata E.N., Pickett J.A., Wadhams J., Woodcock C.M., Mustaparta H. Identification of host and nonhost semiochemicals of eucalyptus woodborer Phoracantha semipunctata by gas chromatography-electroantennography. Journal of Chemical Ecology 2000, 26:1877-1895.
8. Barata E.N., Mustaparta H., Pickett J.A., Wadhams L.J., Araujo J. Encoding of host and non-host plant odours by receptor neurons in the eucalyptus woodborer, Phoracantha semipunctata (Coleoptera: Cerambycidae). Journal of Comparative Physiology 2002, 188:121-133.
9. Binyameen M., Anderson P., Ignell R., Seada M.A., Hansson B.S., Schlyter F. Spatial organization of antennal olfactory sensory neurons in the female Spodoptera littoralis moth: differences in sensitivity and temporal characteristics. Chemical Senses 2012, 37:613-629.
10. Bengtsson J.M., Wolde-Hawariat Y., Khbaish H., Negash M., Jembere B., Seyoum E., Hansson B.S., Larsson M.C., Hillbur Y. Field attractants for Pachnoda interrupta selected by means of GC-EAD and single sensillum screening. Journal of Chemical Ecology 2009, 35:1063-1076.
11. Birkett M.A., Bruce T.J.A., Martin J.L., Smart L.E., Oakley J., Wadhams L.J. Responses of female orange wheat blossom midge, Sitodiplosis mosellana, to wheat panicle volatiles. Journal of Chemical Ecology 2004, 30:1319-1328.
12. Borg-Karlson A.-K., Tengö J., Valterová I., Unelius C.R., Taghizadeh T., Tolasch T., Francke W. (s)-(+)-Linalool, a mate attractant pheromone component in the bee Colletes cunicularius. Journal of Chemical Ecology 2003, 29:1-14.
13. Bruce T.J.A., Wadhams L.J., Woodcock C.M. Insect host location: a volatile situation. Trends in Plant Science 2005, 10:269-274.
14. Bruce T.J.A., Birkett M.A., Blande J., Hooper A.M., Martin J.L., Khambay B., Prosser I., Smart L.E., Wadhams L.J. Response of economically important aphids to components of Hemizygia petiolata essential oil. Pest Management Science 2005, 61:1115-1121.
15. Burckhardt D. Ctenarytaina eucalypti (Maskell) (Hemiptera, Psylloidea) neu für Mitteleuropa mit Bemerkungen zur Blattflohfauna von Eucalyptus. Mitteilungen der Entomologischen Gesellschaft Basel 1998, 48:59-67.
16. Burckhardt D., Santana D.L.Q., Terra A.L., Andrade F.M., Penteado S.R.C., Iede E.T., Morey C.S. Psyllid pests (Hemiptera: Psylloidea) in South American eucalypt plantations. Bulletin de la Société Entomologique Suisse 1999, 72:1-10.
17. Cadahia D. Proximidad de dos nuevos enemigos de los Eucalyptus en Espan á. Bol Serv Plagas 1980, 6:165-192.
18. Campbell C.A.M., Pettersson J., Pickett J.A., Wadhams L.J., Woodcock C.M. Spring migration of damson-hop aphid, Phorodon humuli (Homoptera: Aphididae), and summer host plant-derived semiochemicals released on feeding. Journal of Chemical Ecology 1993, 19:1569-1576.
19. Chang C., Cho I., Li Q.X. Insecticidal activity of basil oil, trans-anethole, estragole, and linalool to adult fruit flies of Ceratitis capitata, Bactrocera dorsalis, and Bactrocera cucurbitae. Journal of Economic Entomology 2009, 102:203-209.
20. Chapman R.F., Bernays E.A., Simpson S.J. Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. Journal of Chemical Ecology 1981, 7:881-888.
21. Collett N. Biology and control of psyllids, and the possible causes for defoliation of Eucalyptus camaldulensis Dehnh., river red gum in south-eastern Australia - a review. Australian Forestry 2001, 64:88-95.
22. Costanzi M., Costanzi J.C., Cocqempot C. Un nouveau psylle sur les Eucalyptus de la Riviera Ligure et de la Côte d'Azur. Premières observations de Ctenarytaina spatulata Taylor dans le Bassin Méditerranéen occidental. Phytoma - La Défense des Végétaux 2003, 566:48-51.
23. Dahlsten D.L., Hansen E.P., Zuparko R.L., Norgaard R.B. Biological control of the blue gum psyllid proves economically beneficial. California Agriculture 1998, 52:35-40.
24. Dahlsten D.L., Rowney D.L., Copper W.A., Tassan R.L., Chaney W.E., Robb K.L., Tjosvold S., Bianchi M., Lane P. Parasitoid wasp controls blue gum psyllid. California Agriculture 1998, 52:31-34.
25. de Bruyne M., Foster K., Carlson J.R. Odor coding in the Drosophila antenna. Neuron 2001, 30:537-552.
26. Den Otter C.J., Van der Goes van Naters W.M. Single cell recordings from tsetse (Glossina m. morsitans) antennae reveal olfactory, mechano- and cold receptors. Physiological Entomology 1992, 17:33-42.
27. Doughty R.W. The Eucalyptus: A Natural and Commercial History of the Gum Tree 2000, The Johns Hopkins University Press, Baltimore, MD, p. 237.
28. Dudareva N., Negre F., Nagegowda D.A., Orlova I. Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Sciences 2006, 25:417-440.
29. Elliott H.J., de Little D.W. Insect Pests of Trees and Timber in Australia 1984, Forestry Commission, Hobart, p. 90.
30. Gill R.J., Oswalt S.M., Veling S.M. Recently introduced pests of Eucalyptus. California Plant Pest and Disease Report 1998, 17:21-24.
31. Guédot C., Millar J.G., Horton D.R., Landolt P.J. Identification of a sex attractant pheromone for male winterform pear psylla, Cacopsylla pyricola. Journal of Chemical Ecology 2009, 35:1437-1447.
32. Guédot C., Horton D.R., Landolt P.J. Sex attraction in Bactericera cockerelli (Hemiptera: Triozidae). Environmental Entomology 2010, 39:1302-1308.
33. Guerin P.M., Stadler E., Buser H.R. Identification of host plant attractants for the carrot fly, Psila rosae. Journal of Chemical Ecology 1983, 9:843-861.
34. Hansson B.S., Larsson M.C., Leal W.S. Green leaf volatile-detecting olfactory receptor neurones display very high sensitivity and specificity in a scarab beetle. Physiological Entomology 1999, 24:121-126.
35. Hardie J., Visser J.H., Piron P.G.M. Peripheral odour perception by adult aphid forms with the same genotype but different host plant preference. Journal of Insect Physiology 1995, 41:91-97.
36. Hern A., Dorn S. A female-specific attractant for the codling moth, Cydia pomonella, from apple fruit volatiles. Naturwissenschaften 2004, 91:77-80.
37. Hodkinson I.D. Biocontrol of eucalyptus psyllid Ctenarytaina eucalypti by the Australian parasitoid Psyllaephagus pilosus: a review of current programmes and their success. Biocontrol News and Information 1999, 20:129-134.
38. Hodkinson D.I. A new introduced species of Ctenarytaina (Hemiptera, Psylloidea) damaging cultivated Eucalyptus parvula (=parvifolia) in Europe. Deutsche Entomologische Zeitschrift 2007, 54:27-33.
39. Hollis D. Australian Psylloidea: Jumping Plantlice and Lerp Insects 2004, Australian Biological Resources Study, Canberra, p. 216.
40. Horton D.R., Guédot C., Landolt P.J. Diapause status of females affects attraction of male pear psylla, Cacopsylla pyricola, to volatiles from female-infested pear shoots. Entomologia Experimentalis et Applicata 2007, 123:185-192.
41. Horton D.R., Guédot C., Landolt P.J. Attraction of male summerform pear psylla to volatiles from female pear psylla: effects of female age, mating status and presence of the host. Canadian Entomologist 2008, 140:184-191.
42. Kristoffersen L., Hallberg E., Wallén R., Anderbrant O. Sparse sensillar array on Trioza apicalis (Homoptera, Triozidae) antennae-an adaptation to high stimulus levels?. Arthropod Structure & Development 2006, 35:85-92.
43. Kristoffersen L., Larsson M.C., Anderbrant O. Functional characteristics of a tiny but specialized olfactory system: olfactory receptor neurons of carrot psyllids (Homoptera: Triozidae). Chemical Senses 2008, 33:759-769.
44. Lapis E.B., Borden J.H. Olfactory discrimination by Heteropsylla cubana (Homoptera: Psyllidae) between susceptible and resistant species of Leucana (Legunimosae). Journal of Chemical Ecology 1993, 19:83-90.
45. Larsson M.C., Leal W.S., Hansson B.S. Olfactory receptor neurons detecting plant odours and male volatiles in Anomala cuprea beetles (Coleoptera: Scarabaeidae). Journal of Insect Physiology 2001, 47:1065-1076.
46. Lopes O., Barata E.N., Mustaparta H., Araújo J. Fine structure of antennal sensilla basiconica and their detection of plant volatiles in the eucalyptus woodborer, Phoracantha semipunctata Fabricius (Coleoptera: Cerambycidae). Arthropod Structure & Development 2002, 31:1-13.
47. Mann R.S., Rouseff R.L., Smoot J., Rao N., Meyer W.L., Lapointe S.L., Robbins P.S., Cha D., Linn C.E., Webster F.X., Tiwari S., Stelinski L.L. Chemical and behavioral analysis of the cuticular hydrocarbons from Asian citrus psyllid, Diaphorina citri. Insect Science 2012, 10.1111/j.1744-7917.2012.01541.x.
48. Murlis J., Willis M.A., Cardé R.T. Spatial and temporal structures of pheromone plumes in fields and forests. Physiological Entomology 2000, 25:211-222.
49. Mustaparta H. Encoding of plant odour information in insects: peripheral and central mechanisms. Entomologia Experimentalis et Applicata 2002, 104:1-13.
50. Nehlin G., Valterová I., Borg-Karlson A.-K. Monoterpenes released from Apiaceae and the egg-laying preferences of the carrot psyllid, Trioza apicalis. Entomologia Experimentalis et Applicata 1996, 80:83-86.
51. Nojima S., Linn C., Morris B., Zhang A.J., Roelofs W. Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. Journal of Chemical Ecology 2003, 29:321-336.
52. Nottingham S.F., Hardie J., Dawson G.W., Hick A.J., Pickett J.A., Wadhams L.J., Woodcock C.M. Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. Journal of Chemical Ecology 1991, 17:1231-1242.
53. Olivares T.S. Ctenarytaina eucalypti (Maskell 1890): El psilido del eucalipto en Chile (Hemiptera: Sternorryncha: Psylloidea: Spondyliaspininae). Gayana (Concepción) 2000, 64:239-241.
54. Paine T.D., Dahlsten D.L., Millar J.G., Hoddle M., Hanks L.M. UC scientists apply IPM techniques to new eucalyptus pests. California Agriculture 2000, 54:8-13.
55. Paine T.D., Steinbauer M.J., Lawson S.A. Native and exotic pests of Eucalyptus: a worldwide perspective. Annual Review of Entomology 2011, 56:181-201.
56. Patt J.M., Sétamou M. Responses of the Asian citrus psyllid to volatiles emitted by the flushing shoots of its rutaceous host plants. Journal of Chemical Ecology 2010, 39:618-624.
57. Pettersson J., Pickett J.A., Pye B.J., Quiroz A., Smart L.E., Wadhams L.J., Woodcock C.M. Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (Homoptera, Aphididae), and other aphids in cereal fields. Journal of Chemical Ecology 1994, 20:2565-2574.
58. Phillips A.K., Appel A.G., Sims S.R. Topical toxicity of essential oils to the German cockroach (Dictyoptera: Blattellidae). Journal of Economic Entomology 2010, 103:448-459.
59. Pichersky E., Gershenzon J. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 2002, 5:237-243.
60. Pickett J.A., Wadhams L.J., Woodcock C.M., Hardie J. The chemical ecology of aphids. Annual Review of Entomology 1992, 37:67-90.
61. Powell G., Hardie J. The chemical ecology of aphid host alternation: how do return migrants find the primary host plant?. Applied Entomology and Zoology 2001, 36:259-267.
62. Purvis G., Chauzat M.P., Segonds-Pichon A., Dunne R. Life history and phenology of the eucalyptus psyllid, Ctenarytaina eucalypti in Ireland. Annals of Applied Biology 2002, 141:283-292.
63. Sant'ana J., Dickens J.C. Comparative electrophysiological studies of olfaction in predaceous bugs Podisus maculiventris and P. nigrispinus. Journal of Chemical Ecology 1998, 24:965-984.
64. Santana, D.L.Q., 2005. Psilídeos em Eucaliptos no Brasil. Embrapa Florestas. Circular Técnica, 109, pp. 1-14.
65. Santana D.L.Q., Burckhardt D. Introduced Eucalyptus psyllids in Brazil. Journal of Forest Research 2007, 12:337-344.
66. Santos P.E.T.D., Geraldi I.O., Garcia J.N. Estimates of genetic parameters of wood traits for sawn timber production in Eucalyptus grandis. Genetics and Molecular Biology 2004, 27:567-573.
67. Schoonhoven L.M., Jermy T., Van loon J.J.A. Insect-Plant Biology: From Physiology to Evolution 1998, Chapman and Hall, London.
68. Silk P.J., Lemay M.A., LeClair G., Sweeney J., MaGee D. Behavioral and electrophysiological responses of Tetropium fuscum (Coleoptera: Cerambycidae) to pheromone and spruce volatiles. Environmental Entomology 2010, 39:1997-2005.
69. Soroker V., Talebaev S., Harari A.R., Wesley S.D. The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae). Journal of Insect Behavior 2004, 17:613-626.
70. Stensmyr M.C., Larsson M.C., Bice S., Hansson B.S. Detection of fruit- and flower-emitted volatiles by olfactory receptor neurons in the polyphagous fruit chafer Pachnoda marginata (Coleoptera: Cetoniinae). Journal of Comparative Physiology A 2001, 187:509-519.
71. Street R.A., Hewitt C.N., Mennicken S. Isoprene and monoterpene emissions from a Eucalyptus plantation in Portugal. Journal of Geophysical Research 1997, 102:15875-15887.
72. Tasin M., Bäckman A.-C., Coracini M., Casado D., Ioriatti C., Witzgall P. Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 2007, 68:203-209.
73. Su C.-Y., Menuz K., Reisert J., Carlson J.R. Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 2012, 492:66-71.
74. Taylor K.L. A new Australian species of Ctenarytaina Ferris and Klyver (Hemiptera: Psyllidae: Spondyliaspidinae) established in three other countries. Australian Journal of Entomology 1997, 36:113-115.
75. Unsicker S.B., Kunert G., Gershenzon J. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Current Opinion in Plant Biology 2009, 12:479-485.
76. Visser J.H., Avé D.A. General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata. Entomologia Experimentalis et Applicata 1978, 24:538-549.
77. Visser J.H., Piron P.G.M. Olfactory antennal responses to plant volatiles in apterous virginoparae of the vetch aphid Megoura viciae. Entomologia Experimentalis et Applicata 1995, 77:37-46.
78. Visser J.H., Piron P.G.M., Hardie J. The aphids' peripheral perception of plant volatiles. Entomologia Experimentalis et Applicata 1996, 80:35-38.
79. Wenninger E.J., Stelinski L.L., Hall D.G. Behavioral evidence for a female produced sex attractant in Diaphorina citri. Entomologia Experimentalis et Applicata 2008, 128:450-459.
80. Wibe A., Mustaparta H. Encoding of plant odours by receptor neurons in the pine weevil (Hylobius abietis) studied by linked gas chromatography-electrophysiology. Journal of Comparative Physiology A 1996, 179:331-344.
81. Wirthensohn M.G., Sedgley M., Jones G.P. Epicuticular wax of juvenile Eucalyptus leaves and headspace analysis of leaf volatiles. Journal of Essential Oil Research 2000, 12:401-411.
82. Yang M.M., Yang C.T., Chao J.T. Reproductive isolation and taxonomy of two Taiwanese Paurocephala species (Homoptera: Psylloidea). Monograph of Taiwan Museum 1986, 6:176-203.
83. Yassaa N., Meklati B.Y., Cecinato A. Evaluation of monoterpenic biogenic volatile organic compounds in ambient air around Eucalyptus globulus, Pinus halepensis and Cedrus atlantica trees growing in Algiers city area by chiral and achiral capillary gas chromatography. Atmospheric Environment 2000, 34:2809-2816.
84. Zhang Q.H., Schlyter F. Olfactory recognition and behavioral avoidance of angiosperm nonhost volatiles by conifer inhabiting bark beetles. Agricultural and Forest Entomology 2004, 6:1-19.
85. Zini C.A., Augusto F., Christensen E., Smith B.P., Caramão E.B., Pawliszyn J. Monitoring biogenic volatile compounds emitted by Eucalyptus citriodora using SPME. Analytical Chemistry 2001, 73:4729-4735.
86. Zini C.A., Augusto F., Christensen E., Caramão E.B., Pawliszyn J. SPME applied to the study of volatile organic compounds emitted by three Species of Eucalyptus in situ. Journal of Agriculture and Food Chemistry 2002, 50:7199-7205.