Abstract
Insect folivores can cause extensive damage to plants. However, different plant species, and even individuals within species, can differ in their susceptibility to insect attack. Polyphenols that readily oxidize have recently gained attention as potential defenses against insect folivores. We tested the hypothesis that variation in oxidizable phenolic concentrations in Eucalyptus foliage influences feeding and survival of Paropsis atomaria (Eucalyptus leaf beetle) larvae. First we demonstrated that oxidizable phenolic concentrations vary both within and between Eucalyptus species, ranging from 0 to 61 mg.g−1 DM (0 to 81% of total phenolics), in 175 samples representing 13 Eucalyptus species. Foliage from six individuals from each of ten species of Eucalyptus were then offered to batches of newly hatched P. atomaria larvae, and feeding, instar progression and mortality of the first and second instar larvae were recorded. Although feeding and survival parameters differed dramatically between individual plants, they were not influenced by the oxidizable phenolic concentration of leaves, suggesting that P. atomaria larvae may have effective mechanisms to deal with oxidizable phenolics. Larvae feeding on plants with higher nitrogen (N) concentrations had higher survival rates and reached third instar earlier, but N concentrations did not explain most of the variation in feeding and survival. The cause of variation in eucalypt herbivory by P. atomaria larvae is therefore still unknown, although oxidizable phenolics could potentially defend eucalypt foliage against other insect herbivores.
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Change history
05 October 2017
Ian Wallis was inadvertently omitted as an author in this study. Ian Wallis assisted with the collection of the leaf samples that were used in this study, and built the chambers that the insects were housed in.
References
Andrew RL, Peakall R, Wallis IR, Wood JT, Knight EJ, Foley WJ (2005) Marker-based quantitatiAlmeidave genetics in the wild?: the heritability and genetic correlation of chemical defenses in Eucalyptus. Genetics 171:1989–1998. doi:10.1534/genetics.105.042952
Andrew RL, Wallis IR, Harwood CE, Henson M, Foley WJ (2007) Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia 153:891–901. doi:10.1007/s00442-007-0784-1
Appel H (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552
Au J, Marsh KJ, Wallis IR, Foley WJ (2013) Whole-body protein turnover reveals the cost of detoxification of secondary metabolites in a vertebrate browser. J Comp Physiol B 183:993–1003. doi:10.1007/s00360-013-0754-3
Barbehenn RV, Constabel PC (2011) Tannins in plant–herbivore interactions. Phytochemistry 72:1551–1565. doi:10.1016/j.phytochem.2011.01.040
Barbehenn RV, Maben RE, Knoester JJ (2008) Linking phenolic oxidation in the midgut lumen with oxidative stress in the midgut tissues of a tree-feeding caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Environ Entomol 37:1113–1118. doi:10.1603/0046-225x(2008)37[1113:Lpoitm]2.0.Co;2
Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen JP (2009a) Hydrolyzable tannins as "quantitative defenses": limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Physiol 55:297–304
Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen JP (2009b) Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition. Oecologia 159:777–788
Barbehenn RV, Niewiadomski J, Pecci C, Salminen J-P (2013) Physiological benefits of feeding in the spring by Lymantria dispar caterpillars on red oak and sugar maple leaves: nutrition versus oxidative stress. Chemoecol 23:59–70. doi:10.1007/s00049-012-0119-5
Bernays EA, Chamberlain D, Mccarthy P (1980) The differential effects of ingested tannic acid on different species of Acridoidea. Entomol Exp Appl 28:158–166
Carne P (1966) Ecological characteristics of the eucalypt-defoliating chrysomelid Paropsis atomaria Ol. Aust J Zool 14:647–672
Close DC, Davies NW, Beadle CL (2001) Temporal variation of tannins (galloylglucoses), flavonols and anthocyanins in leaves of Eucalyptus nitens seedlings: implications for light attenuation and antioxidant activities. Aust J Plant Physiol 28:269–278. doi:10.1071/PP00112
Close D, McArthur C, Paterson S, Fitzgerald H, Walsh A, Kincade T (2003) Photoinhibition: a link between effects of the environment on eucalypt leaf chemistry and herbivory. Ecology 84:2952–2966. doi:10.1890/02-0531
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. doi:10.1126/science.230.4728.895
Cooper SM, Owensmith N (1985) Condensed tannins deter feeding by browsing ruminants in a south African savanna. Oecologia 67:142–146. doi:10.1007/Bf00378466
De Oliveira HG, Molin-Rugama AJ, Fadini MAM, Rezende D, Soto A, Oliveira C, Pallini A (2010) Induced defense in Eucalyptus trees increases with prolonged herbivory. Revista Colomb de Entomol 36:1–4
Fox L, Macauley B (1977) Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia 29:145–162
Fox LR, Morrow PA (1981) Specialization - species property or local phenomenon. Science 211:887–893. doi:10.1126/science.211.4485.887
Gherlenda AN, Haigh AM, Moore BD, Johnson SN, Riegler M (2015) Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species. Oecologia 177:607–617. doi:10.1007/s00442-014-3182-5
Hagerman AE (2012) Fifty years of polyphenol-protein complexes. Recent Advances in Polyphenol Research 3:71–97
Hagerman AE, Ritchard NT, Jones GA, Riechel TL (1996) Tannins in biological redox reactions. American Institute for Cancer Research annual Research conference. August 31 1995:Washington DC
Henery ML, Henson M, Wallis IR, Stone C, Foley WJ (2008a) Predicting crown damage to Eucalyptus grandis by Paropsis atomaria with direct and indirect measures of leaf composition. For Ecol Manag 255:3642–3651. doi:10.1016/j.foreco.2008.03.003
Henery ML, Wallis IR, Stone C, Foley WJ (2008b) Methyl jasmonate does not induce changes in Eucalyptus grandis leaves that alter the effect of constitutive defences on larvae of a specialist herbivore. Oecologia 156:847–859. doi:10.1007/s00442-008-1042-x
Henery ML, Stone C, Foley WJ (2009) Differential defoliation of Eucalyptus grandis arises from indiscriminant oviposition and differential larval survival. Agric Forest Entomol 11:107–114. doi:10.1111/j.1461-9563.2008.00423.x
Herms DA, Mattson WJ (1992) The dilemma of plants - to grow or defend. Q Rev Biol 67:283–335. doi:10.1086/417659
Hillis W (1966) Polyphenols in the leaves of Eucalyptus L'Herit: a chemotaxonomic survey - I. Introduction and a study of the series. Globulares Phytochem 5:1075–1090
Larsson S, Ohmart CP (1988) Leaf age and larval performance of the leaf beetle Paropsis atomaria. Ecol Entomol 13:19–24. doi:10.1111/j.1365-2311.1988.tb00329.x
Lawler I, Foley WJ, Woodrow IE, Cork S (1997) The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109:59–68
Marsh KJ, Wallis IR, Foley WJ (2003) The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula). Aus J Zool 51:31–42
Martin JS, Martin MM, Bernays EA (1987) Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J Chem Ecol 13:605–621
Matsuki M, Foley WJ, Floyd RB (2011) Role of volatile and non-volatile plant secondary metabolites in host tree selection by Christmas beetles. J Chem Ecol 37:286–300. doi:10.1007/s10886-011-9916-5
McArt S, Spalinger D, Collins W, Schoen E, Stevenson T, Bucho M (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central. Alaska Ecol 90:1400–1411
Miles PW, Aspinall D, Correll AT (1982) The performance of two chewing insects on water-stressed food plants in relation to changes in their chemical composition. Aus J Zool 30:347–355. doi:10.1071/Zo9820347
Moore BD, Wallis IR, Wood JT, Foley WJ (2004) Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol Monogr 74:553–568. doi:10.1890/03-4038
Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750. doi:10.1111/nph.12526
Morrow PA, Fox LR (1980) Effects of variation in Eucalyptus essential oil yield on insect growth and grazing damage. Oecologia 45:209–219. doi:10.1007/Bf00346462
Murray TJ, Ellsworth DS, Tissue DT, Riegler M (2013) Interactive direct and plant-mediated effects of elevated atmospheric [CO2] and temperature on a eucalypt-feeding insect herbivore. Glob Chang Biol 19:1407–1416. doi:10.1111/gcb.12142
Nahrung HF, Schutze MK, Clarke AR, Duffy MP, Dunlop EA, Lawson SA (2008) Thermal requirements, field mortality and population phenology modelling of Paropsis atomaria Olivier, an emergent pest in subtropical hardwood plantations. For Ecol Manag 255:3515–3523. doi:10.1016/j.foreco.2008.02.033
Nersesian CL, Banks PB, Simpson SJ, McArthur C (2012) Mixing nutrients mitigates the intake constraints of a plant toxin in a generalist herbivore. Behav Ecol 23:879–888. doi:10.1093/beheco/ars049
Ohmart CP, Edwards PB (1991) Insect herbivory on Eucalyptus. Annu Rev Entomol 36:637–657. doi:10.1146/annurev.en.36.010191.003225
Ohmart CP, Stewart LG, Thomas JR (1985) Effects of food quality, particularly nitrogen concentrations, of Eucalyptus blakelyi foliage on the growth of Paropsis atomaria larvae (Coleoptera: Chrysomelidae). Oecologia 65:543–549. doi:10.1007/Bf00379670
Ohmart CP, Thomas JR, Stewart LG (1987) Nitrogen, leaf toughness and the population-dynamics of Paropsis atomaria Olivier (Coleoptera, Chrysomelidae) - a hypothesis. J Aust Entomol Soc 26:203–207
Östrand F, Wallis IR, Davies NW, Matsuki M, Steinbauer MJ (2008) Causes and consequences of host expansion by Mnesampela privata. J Chem Ecol 34:153–167. doi:10.1007/s10886-007-9422-y
Paine TD, Steinbauer MJ, Lawson SA (2011) Native and exotic pests of Eucalyptus: a worldwide perspective. Annu Rev Entom 56(56):181–201. doi:10.1146/annurev-ento-120709-144817
Rapley LP, Allen GR, Potts BM, Davies NW (2007) Constitutive or induced defences - how does Eucalyptus globulus defend itself from larval feeding? Chemoecol 17:235–243. doi:10.1007/s00049-007-0382-z
Roslin T, Salminen JP (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338
Salminen JP, Lempa K (2002) Effects of hydrolysable tannins on a herbivorous insect: fate of individual tannins in insect digestive tract. Chemoecol 12:203–211
Salminen JP, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711
Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–150. doi:10.1126/science.217.4555.149
Schutze MK, Clarke AR (2008) Converse Bergmann cline in a Eucalyptus herbivore, Paropsis atomaria Olivier (Coleoptera: Chrysomelidae): phenotypic plasticity or local adaptation? Glob Ecol Biogeogr 17:424–431. doi:10.1111/j.1466-8238.2007.00374.x
Slansky F, Feeny P (1977) Stabilization of rate of nitrogen accumulation by larvae of cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228. doi:10.2307/1942617
Steinbauer MJ, Farnier K, Taylor GS, Salminen JP (2016) Effects of eucalypt nutritional quality on the bog gum-Victorian metapopulation of Ctenarytaina bipartita and implications for host and range expansion. Ecol Entomol 41:211–225. doi:10.1111/een. 12295
Tanton M, Epila J (1984) Parasitization of larvae of Paropsis atomaria Ol (Coleoptera: Chrysomelidae) in the Australian Capital Territory. Aus J Zool 32:251–259
Vihakas M, Pälijärvi M, Karonen M, Roininen H, Salminen J-P (2014) Rapid estimation of the oxidative activities of individual phenolics in crude plant extracts. Phytochemistry 103:76–84. doi:10.1016/j.phytochem.2014.02.019
Zhang L, Liu R, Gung BW, Tindall S, Gonzalez JM, Halvorson JJ, Hagerman AE (2016) Polyphenol-aluminum complex formation: implications for aluminum tolerance in plants. J Agric Food Chem 64:3025–3033. doi:10.1021/nnjafc.6b00331
Acknowledgements
Funding was provided by the Australian Research Council to KJM (DE120101263). We thank Dr. ML Henery for help with culture of P. atomaria and Professor J-P Salminen for advice on the oxidizable phenolic assay.
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A correction to this article is available online at https://doi.org/10.1007/s10886-017-0893-1.
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Marsh, K.J., Zhou, W., Wigley, H.J. et al. Oxidizable Phenolic Concentrations Do Not Affect Development and Survival of Paropsis Atomaria Larvae Eating Eucalyptus Foliage. J Chem Ecol 43, 411–421 (2017). https://doi.org/10.1007/s10886-017-0835-y
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DOI: https://doi.org/10.1007/s10886-017-0835-y