Abstract
The capacity to produce carbon-based secondary compounds (CBSC), such as phenolics (including tannins) and terpenes as defensive compounds against herbivores or against neighboring competing plants can be involved in the competition between alien and native plant species. Since the Hawaiian Islands are especially vulnerable to invasions by alien species, we compared total phenolic (TP), total tannin (Tta), and total terpene (TT) leaf contents of alien and native plants on Oahu Island (Hawaii). We analyzed 35 native and 38 alien woody plant species randomly chosen among representative current Hawaiian flora. None of these CBSC exhibited phylogenetic fingerprinting. Alien species had similar leaf TP and leaf Tta contents, and 135% higher leaf TT contents compared with native species. Alien plants had 80% higher leaf TT:N leaf content ratio than native plants. The results suggest that apart from greater growth rate and greater nutrient use, alien success in Oahu also may be linked to greater contents of low cost chemical defenses, such as terpenes, as expected in faster-growing species in resource rich regions. The higher TT contents in aliens may counterbalance their lower investment in leaf structural defenses and their higher leaf nutritional quality. The higher TT provides higher effectiveness in deterring the generalist herbivores of the introduced range, where specialist herbivores are absent. In addition, higher TT contents may favor aliens conferring higher protection against abiotic and biotic stressors. The higher terpene accumulation was independent of the alien species origin, which indicates that being alien either selects for higher terpene contents post-invasion, or that species with high terpene contents are pre-adapted to invasiveness. Although less likely, an originally lower terpene accumulation in Hawaiian than in continental plants that avoids the increased attraction of specialist enemies associated to terpenes may not be discarded.
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Albrectsen, B.R., Gardfjell, H., Orians, C.M., Murray, B., and Fritz, R.S. 2004. Slugs, willow seedlings and nutrient fertilization: intrinsic vigour inversely affects palatability. Oikos 105:268–278.
Allison, S.D., and Vitiusek, P.M. 2004. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619.
Baruch, Z., and Goldstein, G. 1999. Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawai’i. Oecologia 121:183–192.
Beck, S.D., and Schoonhoven, L.M. 1980. Insect behaviour and plant resistance. pp. 115–135. In: Maxwell, F.G., Jennings, P.R. (eds.) Breeding Plant Resistance to Insects. J. Willey and Sons, New York
Bennet, R., and Wallsgrove, R.M. 1994. Secondary metabolites in plant defense mechanisms. New Phytol. 127:617–633,
Bernays, E.A., and Chapman, R.E. 1994. Host Plant Selection by Phytophagus Insects. Chapman and Hall, New York, New York.
Bi, J.L., Felton, G.W., Murphy, J.B., Howles, P.A., Dixon, R.A., and Lamb, C.J. 1997. Do plant phenolics confer resistance to specialist and generalist insect herbivore? J. Agricul. Food Chem. 45:4500–4504.
Blomberg, S.P., Garland, T. Jr., and Ives, A.R. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745.
Blossey, B., and Nötzold, B. 1995. Evolution of increased competitive ability in invasive non indigenous plants: a hypothesis. J. Ecol. 83:887–889.
Blumenthal, D.M., and Hufbauer, R.A. 2007. Increased plant size in exotic populations: a common-garden test with 14 invasive species. Ecology 88:2758–2765.
Boege, K., and Dirzo, R. 2004. Intraspecific variation in growth, defense and herbivory in Dalium guianense (Caesalpiniaceae) mediated by edaphic heterogeneity. Plant Ecol. 175:59–69.
Bryant, J.P., Chapin, F.S. III, and Klein, D.R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368.
Cipollini, D., Stevenson, R., Enright, S., Eyles, A., and Bonello, P. 2008. Phenolic metabolites in leaves of the invasive shrub, Lonicera maackii, and their potential phytotoxic and anti-herbivore effects. J. Chem. Ecol. 34:144–152.
Coley, P. D., Bryant, J. P., and Chapin, F. S. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.
Daehler, C. C., and Baker, R. F. 2006. New records of naturalized and naturalizing plants around Lyon Arboretum, Manoa Valley, Oahu. pp. 3–18. In: Evenhuis, N. L., and Eldredge L. G. (eds). Records of the Hawaii Biological Survey for 2004–2005. Part 1: Articles. Bishop Museum Occasional Papers, 87. Honolulu: Bishop Museum.
Daehler, C. C., Denslow, J. S., Ansari, S., and Kuo, H. F. 2004. A risk assessment system for screening out invasive pest plants from Hawai'i and other Pacific Islands. Conserv. Biol. 18:360–368.
Deenik, J., and Mcclellan, A. T. 2007. Soils of Hawai‘i. Soil and Crop Management, SCM-20. Honolulu: Cooperative Extension Service, College of Tropical Agriculture and Human Resources, University of Hawai'i at Manoa.
Dicke, M., and Baldwin, T. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help”. Trends Plant Sci. in press
Eck, G., Fiala, B., Linsenmair, Hashim, R. B., and Proksh, P. 2001. Trade-off between chemical and biotic antiherbivore defense in the south east Asian plant Genus Macaranga. J. Chem. Ecol. 27:1979–1996
Eichhorn, M. D., Fagan, K. C., Compton, S. G., Dent, D. H., and Hartley, S. E. 2007. Explaining leaf herbivory rates on tree seedlings in a Malasian rain forest. Biotropica 39:416–421.
Filella, I., and Peñuelas, J. 1999. Altitudinal differences in UV absorbance, UV reflectance and related morphological traits of Quercus ilex and Rhododedron ferrugineum in the Mediterranean region. Plant Ecol. 145: 157–162.
Funk, J. L., and Vitousek, P. M. 2007. Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081.
Garland, T. J., Harvey, P. H., and Ives A. R. 1993. Procedures for the analysis of comparative data using phylogenetically independent contrast. Syst. Biol. 41:18–32.
Gershenzon, J., and Duradeva, N. 2007. The function of terpene natural products in the natural world. Nature Chem. Biol. 3:408–414.
Giambelluca, T. W., Nullet, M. A., and Schroeder, T. A. 1986. Rainfall atlas of Hawai'i. Hawa'i Division of Water and Land Development, Department of Land and Natural Resources, Honolulu. 267.
Goverde, M., Bazin, A., Shykoff, J. A., Erhardt, A. 1999. Influence of leaf chemistry of Lotus corniculatus (Fabaceae) on larval development of Polyommatus icarus (Lepidoptera, Lycaenidae): effects of elevated CO2 and plant genotype. Funct. Ecol. 13:801–810.
Hamilton, J.G., Zangerl, A.R., Delucia, E.H., and Berenbaum, M.R. 2001. The carbon.nutrient balance hypothesis: its rise and fall. Ecol. Let. 4:86–95.
Harley, P. C., Litvak, M.E., Sharkey, T. D., and Monson R.K. 1994. lsoprene Emission from Velvet Bean Leaves' lnteractions among Nitrogen Availability, Crowth Photon Flux Density, and Leaf Development. Plant Physiol., 105:279–285.
Harrington, R. A., and Ewel, J. J. 1997. Invasibility of tree plantations by native and non-indigenous plant species in Hawaii. Forest Ecol. Manag. 99:153–162.
Hughes, R.F., and Denslow, J.S. 2005. Invasion by a N2-fixing tree alters function and structure in wet lowland forest of Hawaii. Ecol. Appl. 15:1615–1628.
Hughes, R.F., and Uowolo, A. 2006. Impacts of Falcataria moluccana invasion on decomposition in Hawaiian lowland wet forest: The importance of stand-level controls. Ecosystems 9:977–991.
Hull-Sanders, H. M., Clare, R., Johnson, R. H., and Meyer, G.A. 2007. Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. J. Chem. Ecol. 33:781–799.
Joshi, J., and Vrieling, K. 2005. The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol. Lett. 8:704–714.
Khanh, T. D., Cong, L. C., Xuan, T. D., Lee, S. J., Kong, D. S., and Chung, L. M. 2008. Weed-suppressing potential of dodder (Cuscuta hygrophilae) and its phytotoxic constituients. Weed Sci. 56:119–127.
Koricheva, J. 2002. The carbon-nutrient balance hypothesis is dead; long live the carbon-nutrient balance hypothesis?. Oikos 98:537–539
Kouki, M., and Manetas, Y. 2002. Toughness is less important than chemical composition of Arbutus unedo leaves in food selection by Poecilimon specoes. New Phytol. 154:399–407.
Kurokawa, H., and Nakashizuka, T. 2008. Leaf herbivory and decomposability in a Malaysian tropical rain forest. Ecology 89:2645–2656.
Kursar T. A., and Coley, P.D. 2003. Convergente in defense síndromes of young leaves in tropical rainforests. Biochem. System. Ecol. 31:929–949.
Landau, I., Mullerscharer, H., and Ward, P. I. 1994. Influence of cnicin, a sesquiterpene lactone of Centaurea maculosa (Asteraceae), on specialist and generalist herbivores. J. Chem. Ecol. 20:929–942.
Lankau, R.R. 2007. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol. 175:176–184.
Lavin, S. R., Karasov, W. H., Ives, A. R., Middlrton, K. M., and Garland, T. Jr. 2008. Morphometrics of the avian small intestine compared with that of nonflying mammals: A phylogenetic approach. Physiol. Biochem. Zool. 81:526–550.
Legar, E. A., and Forister, M. L. 2005. Increased resistance to generalist herbivores in invasive populations of the California poppy (Eschscholzia californica). Divers. Distribution 11:311–317.
Lewis, K. C., Bazzaz, F. A., Liao, Q., and Orians, C. M. 2006. Geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata. Oecologia 148:384–395.
Litvak, M. E., Loreto, F., Harley, P. C., Sharkey, T. D., and Monson, R. K. 1996. The response of isoprene emission rate and photosynthetic rate to photon flux and nitrogen supply in aspen and white oak trees. Plant Cell Environ. 19:549–559.
Lodge, D. 1993. Biological invasions, lessons from ecology. Trends Ecol. Evol. 8:133–137.
Mack, M. C., and D’antonio, C. M. 2003. Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol. Appl. 13:154–166.
Makkar H. P. S., and Goodchild A. V. 1996. Quantification of Tannins: A Laboratory Manual. International Center for Agricultural Research in the Dry Areas (ICARDA), Aleppo.
Marigo, G. 1973. Sur une méthode de fractionnement et d’estimation de composes phénoliques chez les végétaux. Analusis 2:106–110.
Mihaliak, C. A., Couvet, D., and Lincoln, D. E. 1987. Inhibition of feeding by a generalist insect due ti increased volatile leaf terpenes under nitrate-limiting conditions. J. Chem. Ecol. 13:2059–2067.
Mole, S., Rogler, J. C., Morell, J., and Butler, L. G. 1990. Herbivore growth reduction by tannins: use of waldbauer ratio techniques and manipulation of salivary protein production to elucidate mechanisms of action. Biochem. Syst. Evol. 18:183–197.
Mooney, H. A., and Hobbs, R. J. 2000. Invasive Species in a Changing World. Island Press. Washington. US. pp. 457.
Mote, T. E., Vullalba, J. J., and Provenza, F. D. 2007. Relative availability of Tannins- and terpene-containing foods affects food intake and preference by lambs. J. Chem. Ecol. 33:1197–1206.
Müller-Dombois, D., and Fosberg, F. R. 1998. Vegetation of the tropical Pacific Islands. New York: Springer Verlag.
Müller-Schärer, H., Schaffner, U., and Steiner, T. 2004. Evolution in invasive plants: implications for biological control. Trends Ecol. Evol. 19:417–422.
Mutikainen, P., Walls, M., Ovaska, J., Kainenen, M., Julknen-Tiito, R., and Vapaavuori, E. 2000. Herbivore resistance in Betula pendula: Effect of fertilization, defoliation and plant genotype. Ecology 8:49–65.
Nitao, J. K., Zangerl, A. R., and Berenbaum, M. R. 2002. CNB: requiescat in pace? Oikos 98:540–546.
Nomura, M., and Itioka, T. 2002. Effects of synthesized tannin on the growth and survival of a generalist herbivorous insect, the common cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Appl. Entomol. Zool. 37:285–289.
Normile, D. 2004. Expanding trade with China creates ecological backlash. Science 306:968–969.
Pattison, R. R., Goldstein, G., and Ares, A. 1998. Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459.
Peñuelas, J., Ribas-Carbó, M., and Giles, L. 1996. Effects of allelochemicals on plant respiration and oxygen isotope fractionation by the alternative oxidase. J. Chem. Ecol. 22:801–805.
Peñuelas, J., and Estiarte, M. 1998. Can elevated CO2 affect secondary metabolism and ecosystem functioning? Trends Ecol. Evol. 13:20–24.
Peñuelas J., and Llusià, J. 2003 BVOCs: Plant defense against climate warming? Trends Plant Sci. 8:105–109.
Peñuelas J., and Llusià J. 2004. Plant VOC emissions: making use of the unavoidable. Trends Ecol. Evol. 19:402–404.
Peñuelas J., and Munné-Bosch, S. 2005. Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci. 10:166–169.
Peñuelas, J., Sardans, J., Llusià, J., Owen, S., Carnicer, J., Giambelluca, T. W., Rezende, E. L., Waite, M., and Niinemets, Ü. 2010. Faster returns on ‘leaf economics’, greater nutrient capture and reduced climate sensitivity in invasive plant species. Global Change Biol. 16:2171–2185.
Peñuelas, J., and Staudt, M. 2010. BVOCs and global change. Trends Plant Sci. 15:133–144.
Pheloung, P. C., Williams, P. A., and Halloy, S. R. P.. 1999. A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. J. Environ Manag. 57:239–251.
Porter, L. J., Hrstich, L.N., and Chang, B.G. 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin, Phytochemistry 25:223–230.
Reich, P. B., Walters, M. B., and Ellswoth, D. S. 1997. From tropics to Tundra: global convergence in plant functioning. Proc. Nat. Acad. Sci. USA 94:13730–13734.
Sardans, J., Llusià, J., Niinemets, Ü., Owen, S., and Peñuelas J. 2010. Foliar Mono- and Sesquiterpene Contents in Relation to Leaf Economic Spectrum in Native and Alien Species in Oahu (Hawaii). J. Chem. Ecol. 36:210–226.
Singleton, V. L., and Rossi, J. A. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Viticulture 16:144–158.
Smith, C. D. 1996. Impact of Alien Plant on Hawai’i’s Native Biota. University of Hawai’i. Botany Department.
Sorensen, J. S., Mclister, J. D., and Dearing, M. D. 2005. Novel plant secondary metabolites impact dietary specialists more than generalist (Neotoma sp.). Ecology 86:140–154.
Stastny, M., Schaffner, U., and Elle, E. 2005. Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J. Ecol. 93:27–37.
Uehara, G., and Ikawa. H. 2000. Use of information from soil surveys and classification. Plant nutrient management in Hawaii’s soils, approaches for tropical and subtropical agriculture. Honolulu: College of Tropical Agriculture and Human Resources, University of Hawai'i at Manoa, 67–77.
Viiri, H., Annila, E., Kitunen, V., and Niemelä, P. 2001. Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15:112–122.
Vitousek, P. M., and Walker, L. R. 1989. Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol. Monogr. 59:247–265.
Wagner, L. R., Herbst, D. R., and Sahmer, S. H. 1999. The Manual of Flowering Plants of Hawai’i (revised edition). University of Hawai’i Press, Honolulu, Hawaiì. pp 1919.
Webb, C. O., and Donoghue, M. J. 2005. Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5:181–183.
Wright, D. M., Jordan, G. J., Lee, W. G., Duncan, R. P., Forsyth, D. M., and Coomes, D. A. 2010. Do leaves of plants on phosphorus-impoverished soils contain high concentrations of phenolic defence compounds? Funct. Ecol. 24:52–61.
Wright, I. J., Reich, P. B., Westoby, M., Ackerly, D. D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J. H. C., Diemer, M., Flexas, J., Garnier, E., Groom, P. K., Gullas, J., Hikosaka, K., Lamont, B. B., Lee, T., Lee, W., Lusk, C., Midgley, J. J., Navas, M. L., Niinemets, Ü., Oleskyn, J., Osada, N., Poorter, H., Poot, P., Prior, P., Pyankov, V.I., Roumet, C., Thomas, S. C., Tjoelker, M. G., Vaneklaas, E. J., and Villar, R. 2004. The worldwide leaf economic spectrum. Nature 428:821–827.
Acknowledgements
We thank Theodore Garland Jr. for providing most of the statistical programs used for phylogenetic analyses. This research was supported by the University of Hawaii (G. P. Wilder research funds), and grants from the Spanish Government (CGL2006-04025/BOS, CGL2010-17172 and Consolider-Ingenio Montes CSD2008-00040), the Catalan Government (SGR 2009-458), the Estonian Ministry of Education and Science (grant SF1090065s07), the Spanish National Research council (CSIC-PIF08-006-3), and the Estonian Science Foundation (grant 7645).
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Peñuelas, J., Sardans, J., Llusia, J. et al. Higher Allocation to Low Cost Chemical Defenses in Invasive Species of Hawaii. J Chem Ecol 36, 1255–1270 (2010). https://doi.org/10.1007/s10886-010-9862-7
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DOI: https://doi.org/10.1007/s10886-010-9862-7