Abstract
Individual Eucalyptus trees in south-eastern Australia vary considerably in susceptibility to herbivores. On the one hand, studies with insect herbivores have suggested that variation in the concentrations of foliar monoterpenes is related to variation in susceptibility. On the other, studies with marsupial folivores have suggested that variation in the concentrations of sideroxylonals (a group of formylated phloroglucinol compounds) is responsible for variation in susceptibility. We examined relative importance of sideroxylonals and 1,8-cineole (a dominant monoterpene) in host tree selection by Christmas beetles (Anoplognathus species: Coleoptera: Scarabaeidae) by using no-choice experiments, choice/no-choice experiments, and manipulative experiments in which concentrations of sideroxylonals or 1,8-cineole were altered. We used two species of host Eucalyptus, one species of non-host Eucalyptus, and three species of non-host non-Eucalyptus trees. Leaf consumption by Christmas beetles was negatively correlated with the concentrations of sideroxylonals and 1,8-cineole. Artificial increases in the concentration of sideroxylonals or 1,8-cineole reduced leaf consumption by Christmas beetles. An artificial reduction in foliar monoterpenes had no effect on leaf consumption by the beetles when leaves contained high or very low concentrations of sideroxylonals. However, when the concentration of sideroxylonals was moderate, a reduction in the foliar monoterpenes increased leaf consumption by the beetles. Therefore, monoterpenes such as 1,8-cineole may be used as a negative cue by Christmas beetles. The pattern of food consumption on non-host Eucalyptus species and non-host non-Eucalyptus species suggest that both positive and negative cues may be used by Christmas beetles to select host trees.
Similar content being viewed by others
References
Andrew, R. L., Wallis, I. R., Harwood, C. E., Henson, M., and Foley, W. J. 2007. Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia 153:891–901.
ASTM. 1995. Standard Practices for Infrared Multivariate Quantitative Analysis Designation (E1655-00). American Society for Testing and Materials, West Conshohocken, Pennsylvania.
Augner, M. 1994. Should a plant always signal its defence against herbivores? Oikos 70:322–332.
Augner, M., and Bernays, E. A. 1998. Plant defence signals and Batesian mimicry. Evolutionary Ecol. 12:667–679.
Ayres, M. P., and MacLean, Jr., S. F. 1987. Development of birch leaves and the growth energetics of Epirrita autumnata (Geometridae). Ecology 68:558–568.
Boland, D. J., Brooker, M. I., Chippendale, G. M., Hall, N., Hyland, B. P., Johnston, R. D., Kleining, D. A., and Turner, J. D. 1984. Forest Trees of Australia, 4th ed. CSIRO Publishing, Melbourne.
Brown, P., Jr. 1993. Measurement, Regression, and Calibration. Clarendon, Oxford.
Carne, P. B., Greaves, R. T. G., and McInnes, R. S. 1974. Insect damage to plantation-grown eucalypts in north coastal New South Wales, with particular reference to Christmas beetles (Coleoptera: Scarabaeidae). Aust. J. Entomol. Soc. 13:189–206.
Cock, M. J. W. 1978. The assessment of preference. J. Animal Ecol. 47:805–816.
DeGabriel, J. L., Moore, B. D., Marsh, K. J., and Foley, W. J. 2010. The effect of plant secondary metabolites on the interplay between the internal and external environments of marsupial folivores. Chemoecology 20:97–108.
Denno, R. F. and McClure, M. S. (eds.). 1983. Variable Plants and Herbivores in Natural and Managed Systems. Academic, New York.
Dethier, V. G., and Post, M. T. 1979. Oligophagy and absence of food-aversion learning in tabacco hornworms, Manduca sexta. Physiol. Entomol. 4:125–130.
Edwards, P. B., Wanjura, W. J., Brown, W. V., and Dearn, J. M. 1990. Mosaic resistance in plants. Nature 347:434.
Edwards, P. B., Wanjura, W. J., and Brown, W. V. 1993. Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95:551–557.
Eisner, T., and Grant, R. P. 1981. Toxicity, odor aversion and ‘olfactory aposematism’. Science 213:476.
Eschler, B. M. and Foley, W. J. 1999. A new sideroxylonal from Eucalyptus melliodora foliage. Aust. J. Chem. 52:157–158.
Eschler, B. M., Pass, D. M., Willis, R., and Foley, W. J. 2000. Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem. Syst. Ecol. 28:813–824.
Feeny, P. P. 1968. Effects of oak leaf tannins on larval growth of the winter oak moth Operophtera brumata. J. Insect Physiol. 14:805–817.
Fritz, R. S., and Simms, E. L. (eds.) 1992. Plant Resistance to Herbivores and Pathogens. University of Chicago Press, Chicago.
Futuyma, D. J. and McCafferty, S. S. 1990. Phylogeny and the evolution of host plant associations in the leaf beetle genus Ophraella (Coleoptera, Chrysomelidae). Evolution 44:1885–1913.
Genstat 5 Committee. 1993. Genstat 5 Release 3, Reference manual. Oxford University Press, Oxford.
Ghisalberti, E. L. 1996. Bioactive acylphloroglucinol derivatives from Eucalyptus species. Phytochemistry 41:7–22.
Gleadow, R. M., Haburjak, J., Dunn, J. E., Conn, M. E., and Conn, E. E. 2008. Frequency and distribution of cyanogenic glycosides in Eucalyptus L’Hérit. Phytochemistry 69: 1870–1874.
Guilford, T. and Cuthill, I. 1991. The evolution of aposematism in marine gastropods. Evolution 45:449–451.
Hunter, M. D. 1997. Incorporating variation in plant chemistry into a spatially explicit ecology of phytophagous insects, pp. 81–96, in A. D. Watt, N. E. Stork, and M. D. Hunter (eds.). Forests and Insects. Chapman and Hall, London.
Infrasoft International. 1996. NIRS 3, version 4.00. Routine Operation, Calibration Development, and Network System Management Software for Near Infrared Instruments. NIRSystems, Inc., Silver Spring, Meryland.
Jacobs, J. 1974. Quantitative measurement of food selection. A modification of the forage ratio and Ivlev’s electivity index. Oecologia 14:413–417.
Janz, N. and Nylin, S. 1998. Butterflies and plants: a phylogenetic study. Evolution 52:486–502.
Janz, N., Nyblom, K., and Nylin, S. 2001. Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini. Evolution 55:783–796.
Kam, M., Khokhlova, I. S., and Degen, A. A. 1997. Granivory and plant selection by desert gerbils of different body size. Ecology 78:2218–2229.
Launchbaugh, K. L., and Provenza, F. D. 1993. Can plants practice mimicry to avoid grazing by mammalian herbivores? Oikos 66:501–504.
Lawler, I. R., Foley, W. J., Eschler, B. M., Pass, D. M., and Handasyde, K. 1998. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160–169.
Lawler, I. R., Stapley, J., Foley, W. J., and Eschler, B. M. 1999. Ecological example of conditioned flavor aversion in plant-herbivore interactions: Effect of terpenes of Eucalyptus on feeding by common ringtail and brushtail possums. J. Chem. Ecol. 25:401–415.
Lawler, I. R., Foley, W. J., and Eschler, B. M. 2000. Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81:1327–1338.
Leimar, O., and Tuomi, J. 1998. Synergistic selection and graded traits. Evolutionary Ecol. 12:59–71.
Matsuki, M. and MacLean, Jr., S. F. 1994. Effects of different leaf traits on growth rates of insect herbivores on willows. Oecologia 100:141–152.
Matsuki, M., Ayres, M. P., and MacLean, Jr., S. F. 1994. Effects of temperature on growth and molt of Nematus calais (Hymenoptera: Tenthredinidae). Environ. Entomol. 23:719–725.
Matsuki, M., Kay, N., Serin, J., and Scott. J. K. 2010. Variation in the ability of larvae of phytophagous insects to develop on evolutionarily unfamiliar plants: a study with gypsy moth Lymantria dispar and Eucalyptus. Agric. For. Entomol. doi:10.1111/j.1461-9563.2010.00492.x
Moore, B. D., Foley, W. J., Wallis, I. R., Cowling, A., and Handasyde, K. A. 2004a. Eucalyptus foliar chemistry explains selective feeding by koalas. Biol. Lett. 22:64–67.
Moore, B. D., Wallis, I. R., Palá-Paúl, J., Brophy, J. J., Willis, R. H., and Foley, W. J. 2004b. Antiherbivore chemistry of Eucalyptus—Cues and deterrents for marsupial folivores. J. Chem. Ecol. 30:1743–1769.
Morrow, P. A., and Fox, L. R. 1980. Effects of variation in Eucalyptus essential oil yield on insect growth and grazing damage. Oecologia 45:209–219.
Murphy, S. M., and Feeny, P. (2006) Chemical facilitation of a naturally occurring host shift by Papilio machaon butterfly (Papilionidae). Ecol. Monographs 76:399–414.
Ohmart, C. P., and Larsson, S. 1989. Evidence for absorption of eucalypt essential oils by Paropsis atomaria Olivier (Coleoptera: Chrysomelidae). J. Aust. Entomol. Soc. 28:201–205.
Osier, T. L., Hwang, S.-Y., and Lindroth, R. L. 2000. Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol. Entomol. 25:197–207.
Östrand, F., Wallis, I. R., Davies, N. D., Matsuki, M., and Steinbauer, M. J. 2008. Causes and consequences of host expansion by Mnesampela privata. J. Chem. Ecol. 34:153–167.
Pass, D. M., Foley, W. J., and Bowden, B. 1998. Vertebrate herbivory on Eucalyptus—Identification of specific feeding deterrents for common ringtail possums (Pseudocheirus peregrinus) by bioassay-guided fractionation of Eucalyptus ovata foliage. J. Chem. Ecol. 24:1513–1527.
Rose, H. A. 1985. The relationship between feeding specialization and host plants to aldrin epoxidase activities of midgut homogenates in larval Lepidoptera. Ecol. Entomol. 10:455–467.
SAS Institute. 1989. SAS users Guide. Release 6.09 edition. SAS Institute, Cary, North Carolina.
Southwell, I. A., Russell, M. F., Maddox, C. D., and Wheeler, G. S. 2003. Differential metabolism of 1,8-cineole in insects. J. Chem. Ecol. 29:83–94.
Stapley, J., Foley, W. J., Cunningham, R., and Eschler, B. 2000. How well can brushtail possums regulate their intake of Eucalyptus toxins? J. Comp. Physiol. B 170:211–218.
Steinbauer, M. J., and Matsuki, M. 2004. Suitability of Eucalyptus and Corymbia for Mnesampela privata (Guenée) (Lepidoptera: Geometridae) larvae. Agric. For. Entomol. 6:323–332.
Steinbauer, M. J., and Wanjura, W. J. 2002. Christmas beetles (Anoplognathus spp., Coleoptera, Scarabaeidae) mistake peppercorn trees for eucalypts. J. Nat. Hist. 36:119–125.
Steinbauer, M. J., Schiestl, F. P., and Davies, N. W. 2004. Monoterpenes and epicuticular waxes help female autumn gum moth differentiate between waxy and glossy Eucalyptus and leaves of different ages. J. Chem. Ecol. 30:1117–1142.
Stone, C., and Bacon, P. E. 1994. Relationships among moisture stress, insect herbivory, foliar cineole content and the growth of river red gum Eucalyptus camaldulensis. J. App. Ecol. 31:604–612.
Tuomi, J., and Augner, M. 1993. Synergistic selection of unpalatability in plants. Evolution 47:668–672.
Vickers, N. J., Christiansen, T. A., and Hildebrand, J. G. 1998. Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400:35–56.
Waldbauer, G. P. 1968. The consumption and utilization of food by insects. Adv. Insect Physiol. 5:229–288.
Wallis, I. R., Watson, M. L., and Foley, W. J. 2002. Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Aust. J. Zool. 50:507–519.
Watson, M. L. 1998. Interactions between the common brushtail possum (Trichosurus vulpecula) and Eucalyptus: evaluating natural resistance as a method of pest control in Eucalyptus plantations. Unpublished BSc Honours thesis. Australian National University, Canberra.
Acknowledgements
We thank J. Dowse, R. Sutherland, M. Ebbers, W. Wanjura, G. Farrell, B. Clarke, B. Eschler, I. Lawler, and M. Michie for technical advice, assistance, and discussions. B. Eschler provided purified sideroxylonals. Comments by R. Andrew, S. Cunningham, P. Gullan, P. Edwards, T. Heard, A. Keszei, M. Steinbauer, and anonymous reviewers improved the manuscript. We also thank the late K. Barker, the late H. Healey, and S. Dwyer for granting permission to collect leaves on their properties. P. Edwards provided the historical record of Christmas beetle defoliation. M. Watson, B. Moore, and I. Lawler shared their knowledge of the susceptibility of some Eucalyptus trees to marsupial folivores. Financial support was provided by Rural Industries Research & Development Corporation and Agriculture, Fisheries, and Forestry—Australia. This paper is dedicated to the late Kevin Barker who has noticed a mosaic tree.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuki, M., Foley, W.J. & Floyd, R.B. Role of Volatile and Non-Volatile Plant Secondary Metabolites in Host Tree Selection by Christmas Beetles. J Chem Ecol 37, 286–300 (2011). https://doi.org/10.1007/s10886-011-9916-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-011-9916-5