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Influence of epicuticular-wax composition on the feeding pattern of a phytophagous insect: implications for host resistance

Published online by Cambridge University Press:  02 April 2012

Simon P. Daoust ,
Brian J. Mader ,
Eric Bauce ,
Emma Despland ,
Audrey Dussutour  and
P.J. Albert
Simon P. Daoust
Affiliation:
Institut de Recherche en Biologie Végétale, Université de Montréal, 4101 Sherbrooke Street East, Montréal, Quebec, Canada H1X 2B2
Brian J. Mader
Affiliation:
Department of Biology, Loyola Campus, Concordia University, 7141 Sherbrooke Street West, Montréal, Quebec, Canada H4B 1R6
Eric Bauce*
Affiliation:
Département des sciences du bois et de la forêt, Université Laval, Québec, Canada G1K 7P4
Emma Despland
Affiliation:
Department of Biology, Loyola Campus, Concordia University, 7141 Sherbrooke Street West, Montréal, Quebec, Canada H4B 1R6
Audrey Dussutour
Affiliation:
Research Centre on Animal Cognition, Université Paul Sabatier, Bâtiment 4R3, Unité Mixte de Recherche 5169, Centre National de la Recherche Scientifique, 118 route de Narbonne, Cédex 31062 Toulouse, France
P.J. Albert
Affiliation:
Department of Biology, Loyola Campus, Concordia University, 7141 Sherbrooke Street West, Montréal, Quebec, Canada H4B 1R6
*
1 Corresponding author (e-mail: Eric.Bauce@vrex.ulaval.ca).
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Abstract

A white spruce, Picea glauca (Moench) Voss (Pinaceae), plantation in southern Quebec was found to contain two distinct types of trees, the first resistant and the second susceptible to attack by spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). To identify the mechanisms of white spruce resistance to spruce budworm, we studied the role of epicuticular waxes, comparing (i) the foliar chemistry of susceptible and resistant trees and (ii) the feeding pattern of larvae at first contact with the foliage. Needles collected from resistant trees contained concentrations of the monoterpenes α-pinene and myrcene that were 307% and 476%, respectively, above those found in needles collected from susceptible trees. Although there were no significant differences in probing behaviour, significantly fewer larvae transitioned from probing to feeding on resistant needles; this led to fewer feeding bouts as well as a significantly shorter first meal. Removal of waxes increased the number of individuals transitioning from probing to feeding on resistant needles; this led to more feeding bouts. Our results demonstrate that monoterpenes influence the pattern of feeding of spruce budworm larvae as well as playing an important role in white spruce resistance.

Résumé

Une plantation d'épinette blanche, Picea glauca (Moech) Voss (Pinaceae), composée d'arbres résistants et susceptibles à la tordeuse de bourgeons d'épinette, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae) a été utilisée comme modèle pour investiguer le rôle des cires épicuticulaires dans les mécanismes de résistance des arbres hôtes à la tordeuse. Ainsi, cette approche nous a permis (i) d'étudier les relations entre la composition chimique des cires épicuticulaires des aiguilles et le comportement de palpage et d'ingestion des larves de tordeuse ainsi (ii) que d'analyser le patron d'alimentation de la tordeuse sur le foliage. Les aiguilles provenant d'arbres résistants contenaient respectivement 307 % et 476 % plus d'α-pinene et de myrcene que celles provenant des arbres susceptibles. Aucune différence significative dans le comportement de palpage des aiguilles n’a été détectée. Par contre, moins d'insectes, et cela de manière significative, ont passé de la phase de palpage à la phase d'ingestion lorsqu’en présence d'aiguilles provenant d'arbres résistants. Ce phénomène s’est traduit par une réduction du nombre de périodes d'ingestion et une réduction de la durée du premier repas dans le cas des insectes en présence d'aiguille d'arbres résistants. Lorsque les cires épicuticulaires ont été enlevées, le nombre de tordeuse qui ont passé de la phase de palpage à la phase d'ingestion a augmenté sur les aiguilles provenant d'arbres résistants. Nos résultats démontrent que les monoterpènes semblent influencer le patron d'alimentation de la tordeuse ainsi que jouer un rôle important dans la résistance de l'épinette blanche à la tordeuse.

Type
Articles
Information
The Canadian Entomologist , Volume 142 , Issue 3 , June 2010 , pp. 261 - 270
Copyright
Copyright © Entomological Society of Canada 2010

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References

Ascoli, A., and Albert, P.J. 1985. Orientation behavior of second-instar larvae of eastern spruce budworm Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae) in a Y-type olfactometer. Journal of Chemical Ecology, 11: 837–846. doi:10.1007/BF01012072.CrossRefGoogle Scholar
Bauce, E. 1996. One and two years impact of commercial thinning on spruce budworm feeding ecology and host tree foliage production and chemistry. Forestry Chronicle, 72: 1–6.CrossRefGoogle Scholar
Bauce, E., and Hardy, Y. 1988. Effects of drainages and severe defoliation on the raw fiber content of balsam fir needles and growth of the spruce budworm (Lepidoptera: Tortricidae). Environmental Entomology, 17: 671–674.CrossRefGoogle Scholar
Bauce, E., and Kumbasli, M. 2007. Natural resistance of fast growing white spruce, Picea glauca (Moench), trees against spruce budworm, Choristoneura fumiferana (Clem.). In Bottlenecks, Solutions, and Priorities in the Context of Functions of Forest Resources: Proceedings of the International Symposium, Istanbul, Turkey, 17–19 October 2007. Edited by Demir, M. and Yilmaz, E.. Tubitak Istanbul, Ankara, Turkey. pp. 687–695.Google Scholar
Bauce, E., Crépin, M., and Carisey, N. 1994. Spruce budworm growth, development and food utilization on young and old balsamfir trees. Oecologia, 97: 499–507. doi:10.1007/BF00325888.CrossRefGoogle Scholar
Bauce, E., Bidon, Y., and Berthiaume, R. 2002. Effects of food nutritive quality and Bacillus thuringiensis on feeding behavior, food utilisation and larval growth of spruce budworm Choristoneura fumiferana (Clem) when exposed as fourth and sixth instar. Agricultural and Forest Entomology, 4: 57–70. doi:10.1046/j.1461-9563.2002.00123.x.CrossRefGoogle Scholar
Bernays, E.A., and Chapman, R.F. 1994. Hostplant selection by phytophagous insects. Chapman and Hall, New York.CrossRefGoogle Scholar
Cates, R.G., Henderson, C., and Redak, R. 1987. Responses of western spruce budworm to varying levels of nitrogen and terpenes. Oecologia, 73: 312–316. doi:10.1007/BF00377524.CrossRefGoogle ScholarPubMed
Chapman, R.F. 2003. Contact chemoreception in feeding by phytophagous insects. Annual Review of Entomology, 48: 455–484. PMID:12414737 doi:10.1146/annurev.ento.48.091801.112629.CrossRefGoogle ScholarPubMed
Chapman, R.F., and Sword, G. 1993. The importance of palpation in food selection by a polyphagous grasshopper (Orthoptera: Acrididae). Journal of Insect Behavior, 6: 79–95. doi:10.1007/BF01049149.CrossRefGoogle Scholar
Chen, Z., Kolb, T.E., and Clancy, K.M. 2002. The role of monoterpenes in resistance of Douglas fir to western spruce budworm defoliation. Journal of Chemical Ecology, 28: 897–920. PMID:12049230 doi:10.1023/A:1015297315104.CrossRefGoogle ScholarPubMed
Clancy, K.M., Itami, J.K., and Huebner, D.P. 1991. Douglas-fir nutrients and terpenes: potential resistance factors to western spruce budworm defoliation. Forest Science, 39: 78–94.Google Scholar
Dement, W.A., and Mooney, H.A. 1974. Seasonal variation in the production of tannins and cyanogenic glucosides in the chaparral shrubs, Heteromeles arbutifolia. Oecologia, 15: 65–76. doi:10.1007/BF00345228.CrossRefGoogle ScholarPubMed
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., and Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28: 350–356. doi:10.1021/ac60111a017.CrossRefGoogle Scholar
Dussourd, D.E. 1993. Foraging with finesse: caterpillar adaptations for circumventing plant defenses. In Caterpillars: ecological and evolutionary constraints on foraging. Edited by Stamp, N.E. and Casey, T.M.. Chapman and Hall, New York. pp. 92–123.Google Scholar
Fischer, N.H., Williamson, G.B., Weidenhamer, J.D., and Richardson, D.R. 1994. In search of allelopathy in the Florida scrub: the role of terpenoids. Journal of Chemical Ecology 20: 1355–1380. doi:10.1007/BF02059812.CrossRefGoogle ScholarPubMed
Frazier, J.L., and Chyb, S. 1995. Use of feeding inhibitors in insect control. In Regulatory mechanisms in insect feeding. Edited by Chapman, R. and de Boer, G.. Chapman and Hall, New York. pp. 364–383.CrossRefGoogle Scholar
Gershenzon, J. 1994. The cost of plant chemical defense against herbivory: a biochemical perspective. In Insect–plant interactions. Vol. 5. Edited by Bernays, E.A.. CRC Press, Boca Roton, Florida. pp. 105–173.Google Scholar
Gershenzon, J., and Croteau, R. 1991. Terpenoids.In Herbivores: their interactions with secondary metabolites. Vol. 1. The chemical participants. Edited by Rosenthal, G.A. and Berenbaum, M.R.. Academic Press, New York. pp. 165–219.Google Scholar
Grisdale, D.G., and Wilson, G.G. 1988. A laboratory method of mass rearing the eastern spruce budworm Choristoneura fumiferana. In Advances and challenges in insect rearing. Edited by King, E.G. and Leppla, N.C., United States Department of Agriculture Technical Bulletin, pp. 223–231.Google Scholar
Hagerman, A.E. 1987. Radial diffusion method for determining tannin in plant extracts. Journal of Chemical Ecology, 13: 437–449. doi:10.1007/BF01880091.CrossRefGoogle ScholarPubMed
Hanover, J.W. 1975. Physiology of tree resistance to insects. Annual Review of Entomology, 20: 75–90. doi:10.1146/annurev.en.20.010175.000451.CrossRefGoogle Scholar
Hanover, J.W. 1992. Applications of terpene analysis in forest genetics. New Forest, 6: 159–178.CrossRefGoogle Scholar
Johnson, R.H., Young, B.L., and Alstad, D.N. 1997. Responses of ponderosa pine growth and volatile terpene concentrations to manipulation of soil water and sunlight availability. Canadian Journal of Forest Research, 27: 1794–1804.doi:10.1139/cjfr-27-11-1794.CrossRefGoogle Scholar
Litvak, M.A., and Monson, R.K. 1998. Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia, 114: 531–540. doi:10.1007/s004420050477.CrossRefGoogle ScholarPubMed
Maloney, P.J., Albert, P.J., and Tulloch, A.P. 1988. Influence of epicuticular waxes from white spruce and balsam fir on feeding behavior of the eastern spruce budworm. Journal of Insect Behavior 1: 197–209. doi:10.1007/BF01052238.CrossRefGoogle Scholar
McClure, M., and Hare, J.D. 1984. Foliar terpenoids in Tsuga species and the fecundity of scale insects. Oecologia, 63: 185–193. doi:10.1007/BF00379876.CrossRefGoogle ScholarPubMed
McKinnon, M.L., Quiring, D.T., and Bauce, E. 1998. Influence of resource availability on growth and foliar chemistry within and among young white spruce trees. EcoScience, 5: 295–305.CrossRefGoogle Scholar
Mitchell, R. 1981. Insect behavior, resource exploitation, and fitness. Annual Review of Entomology, 26: 373–396. doi:10.1146/annurev.en.26.010181.002105.CrossRefGoogle Scholar
Muller, C., and Riederer, M. 2005. Plant surface properties in chemical ecology. Journal of Chemical Ecology 31: 2621–2651. PMID:16273432 doi:10.1007/s10886-005-7617-7.CrossRefGoogle ScholarPubMed
Palermo, B.L., Clancy, K.M., and Koch, G.W. 2003. Feeding and oviposition behavior do not explain Douglas-fir resistance to defoliation by the western spruce budworm (Lepidoptera: Tortricidae). Environmental Entomology 32: 626–632. doi:10.1603/0046-225X-32.3.626.CrossRefGoogle Scholar
Pruegel, B., and Lognay, G. 1996. Composition of the cuticular waxes of Picea abies and P. sitchensis. Phytochemical Analysis, 7: 29–36. doi:10.1002/(SICI)1099-1565(199601)7:1,(29::AID-PCA278).3.0.CO;2-L.3.0.CO;2-L>CrossRefGoogle Scholar
Redak, R., and Cates, R.G. 1984. Douglas-fir (Pseudostuga menziesii)-spruce budworm (Choristoneura occidentalis) interactions: the effect of nutrition, chemical defenses, tissue phenology, and tree physical parameters on budworm success.Oecologia, 62: 61–67. doi:10.1007/BF00377374.CrossRefGoogle Scholar
Rivet, M.P., and Albert, P.J. 1990. Ovipistion behavior in spruce budworm Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). Journal of Insect Behaviour. 3: 395–400.CrossRefGoogle Scholar
Roitto, M., Rautio, P., Markkola, A., Julkunen-tiito, R., Varama, M., Saravesi, K., and Tuomi, J. 2009. Induced accumulation of phenolics and sawfly performance in Scots pine response to previous defoliation. Tree Physiology, 29: 207–216. PMID:19203946 doi:10.1093/treephys/tpn017.CrossRefGoogle ScholarPubMed
SAS Institute Inc. 2003. SAS/STAT user's guide. Release 9.1 ed. SAS Institute Inc., Cary, North Carolina.Google Scholar
Simpson, S.J. 1995. Regulation of a meal: chewing insects. In Mechanisms in insect feeding. Edited by Chapman, R. and de Boer, G.Chapman and Hall, New York. pp. 137–156.Google Scholar
Sokal, R.R., and Rohlf, F.J. 1995. Biometry. 3rd ed. W.H. Freeman and Company, New York.Google Scholar
SPSS Inc. 1999. SPSS® version 10.0.0 [computer program]. SPSS Inc., Chicago.Google Scholar
Städler, E. 1986. Oviposition and feeding stimuli in leaf surface waxes. In Insects and the plant surface. Edited by Juniper, B.E. and Southwood, T.R.E.. Edward Arnold Ltd., London, United Kingdom. pp. 106–121.Google Scholar
Städler, E. 1992. Behavioral responses of insects to plant secondary compounds. In Herbivores: their interactions with secondary plant metabolites. Edited by Rosenthal, G.A. and Berenbaum, M., Academic Press, San Diego, California.pp. 45–88.CrossRefGoogle Scholar
Sturgeon, K.B. 1979. Monoterpene variation in ponderosa pine xylem resin related to western pine beetle predation. Evolution, 33: 803–814. doi:10.2307/2407647.CrossRefGoogle ScholarPubMed
Swain, T., and Hillis, W.E. 1959. The phenolic constituents of Prunus domestica I. The quantitative analysis of phenolic constituents. Journal of the Science of Food and Agriculture, 10: 63–68. doi:10.1002/jsfa.2740100110.CrossRefGoogle Scholar
von Rudloff, E., and Rehfeldt, G.E. 1980. Chemosystematics studies in the genus Pseudotsuga. IV. Inheriance and geographic variation in the leaf oil terpenes of Douglas-fir for the Pacific Northwest. Canadian Journal of Forest Research, 58: 546–556.Google Scholar
Wisdom, C.S., Gonzales-Coloma, A., and Rundel, P.W. 1987. Ecological tannin assays: evaluation of proanthocyanidins, protein binding assays and protein precipitating potential. Oecologia, 72: 395–401. doi:10.1007/BF00377570.CrossRefGoogle ScholarPubMed
Woodhead, S., and Chapman, R.F. 1986. Insect behaviour and the chemistry of plant surface waxes. In Insects and the plant surface. Edited by Juniper, B.E. and Southwood, T.R.E.. Edward Arnold, Ltd., London, United Kingdom. pp.123–135.Google Scholar
Wright, G.A., Simpson, S.J., Raubenheimer, D., and Stevenson, P. 2003. The feeding behavior of the weevil, Exopthalmus jekelianus, with respect to the nutrients and allelochemicals in the host plant leaves. Oikos, 100: 172–184. doi:10.1034/j.1600-0706.2003.11270.x.CrossRefGoogle Scholar