Journal of Chemical Ecology

, Volume 36, Issue 2, pp 210–226 | Cite as

Foliar Mono- and Sesquiterpene Contents in Relation to Leaf Economic Spectrum in Native and Alien Species in Oahu (Hawai’i)

  • Jordi SardansEmail author
  • Joan Llusià
  • Ülo Niinemets
  • Sue Owen
  • Josep Peñuelas


Capacity for terpene production may confer advantage in protection against abiotic stresses such as heat and drought, and also against herbivore and pathogen attack. Plant invasive success has been intense in the Hawaiian islands, but little is known about terpene content in native and alien plant species on these islands. We conducted a screening of leaf terpene concentrations in 35 native and 38 alien dominant plant species on Oahu island. Ten (29%) of the 35 native species and 15 (39%) of the 38 alien species contained terpenes in the leaves. This is the first report of terpene content for the ten native species, and for 10 of the 15 alien species. A total of 156 different terpenes (54 monoterpenes and 102 sesquiterpenes) were detected. Terpene content had no phylogenetic significance among the studied species. Alien species contained significantly more terpenes in leaves (average ± SE = 1965 ± 367 μg g−1) than native species (830 ± 227 μg g−1). Alien species showed significantly higher photosynthetic capacity, N content, and lower Leaf Mass Area (LMA) than native species, and showed higher total terpene leaf content per N and P leaf content. Alien species, thus, did not follow the expected pattern of “excess carbon” in comparison with native species. Instead, patterns were consistent with the “nutrient driven synthesis” hypothesis. Comparing alien and native species, the results also support the modified Evolution of Increased Competitive Ability (EICA) hypothesis that suggests that alien success may be favored by a defense system based on an increase in concentrations of less costly defenses (terpenes) against generalist herbivores.


Hawaiian Islands Terpene content Nitrogen Phosphorus Alien species Native species LMA Photosynthetic capacity Monoterpenes Sesquiterpenes Nutrient driven hypothesis “Excess carbon” hypothesis Modified EICA hypothesis 



ÜN was holding G. P. Wilder Chair at the Department of Botany, University of Hawai’i at Manoa, Hawai’i during the time of the study. We also thank the students, faculty, and staff of that Department for making available laboratory space and equipment for this research. This research was supported by grants from the Spanish Government (CGL2006-04025/BOS and Consolider-Ingenio Montes CSD 2008-00040), the Catalan Government (SGR 2009-458), Estonian Science Foundation (grant 7645), and the Estonian Ministry of Education and Science (SF1090065s07).


  1. Allison, S. D., and Vitousek ,P. M. 2004. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619.CrossRefPubMedGoogle Scholar
  2. Barney, J. N., Hay, A. G., and Weston, L. A. 2005. Isolation and characterization of allelopathic volatiles from mugwort (Artemisia vulgaris). J. Chem. Ecol. 31:247–265.Google Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.PubMedGoogle Scholar
  5. Blossey, B., and Nötzold, B. 1995. Evolution of increased competitive ability in invasive non indigenous plants: a hypothesis. J. Ecol. 83:887–889.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. Cao, G., Giambelluca, T., Stevens, B., and Schroeder, T. A. 2007. Inversion variability in the Hawaiian trade wind regime. J. Clim. 20:1145–1160.CrossRefGoogle Scholar
  8. Chang, C. W., Wu, T. S., Hsieh, Y. S., Kuo, S. C., and Chao, P. D. L. 1999. Terpenoids of Syzygium formosanum. J. Nat. Prod. 62:327–328.CrossRefPubMedGoogle Scholar
  9. Chao, L. K., Hua, K. F., Hsu, H. Y., Cheng, S. S., Liu ,J. Y., and Chang S. T. 2005. Study of the anti-inflammatory activity of essential oil from leaves of Cinnamomum osmophloeum. J. Agric. Food Chem. 53:7274–7278.CrossRefPubMedGoogle Scholar
  10. Chiang, Y. M., and Kuo, Y. H. 2002. Novel triterpenoids from aerial roots of Ficus microcarpa. J.Org. Chem. 67:7656–7661.CrossRefPubMedGoogle Scholar
  11. Copolovici, L., Filellai, I., Llusià, J., Niinemets, U., and Peñuelas, J. 2005. The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol. 139:485–496.CrossRefPubMedGoogle Scholar
  12. Daehler, C. C. 2005. Upper-montane plant invasions in the Hawaiian Islands: Patterns and opportunities. Perspect. Plant Ecol. Evol. System. 7:203–216.CrossRefGoogle Scholar
  13. Daehler, C. C., and Baker, R. 2006. Part 1: Articles, pp. 3–18, in N. L. Evenhuis, and L. G. Eldredge (eds.). Records of the Hawaii Biological Survey for 2004–2005, Bishop Museum occasional papers, 87. Bishop Museum, Honolulu.Google Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.Google Scholar
  16. Dewalt, S. J., Denslow, J. S., and Ickes, K. 2004. Natural-enemy releasse facilitates habitat expansion of the invasive tropical shrub Clidemia hista. Ecology 85:471–483.CrossRefGoogle Scholar
  17. Dunbar-co, S., Sporck, M. J., and Sack, L. 2009. Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. Inter. J. Plant Sci.170: 61–75.CrossRefGoogle Scholar
  18. Fernàndez, F., and Torres, M. 2006. Evaluation of Pluchea carolinensis extracts as antioxidants by the epinephrine oxidation method. Fitoterapia 77:221–226.CrossRefPubMedGoogle Scholar
  19. Funk, J. L., and Vitousek, P. M. 2007. Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081.CrossRefPubMedGoogle Scholar
  20. Ghisalberti, E. L. 2000. Lantana camara L. (Verbenaceae). Fitoterapia 71:467–486.CrossRefPubMedGoogle Scholar
  21. Giambelluca, T. W., Nullet, M. A., and Tschroeder, T. A. 1986. Rainfall Atlas of Hawai’i. Hawa’i Division of Water and Land Development, Department of Land and Natural Resources, Honolulu. 267.Google Scholar
  22. Harley, P. C., Litvak, M. E., Sharkey, T. D., and Monsom R. K. 1994. lsoprene Emission from Velvet Bean Leaves’ interactions among Nitrogen Availability, Growth Photon Flux Density, and Leaf Development. Plant Physiol. 105:279–285.PubMedGoogle Scholar
  23. Harrington, R. A., and Ewel, J. J. 1997. Invasibility of tree plantations by native and non-indigenous plant species in Hawaii. For. Ecol. Manag. 99:153–162.Google Scholar
  24. Herms, D. A., and Mattson, W. J. 1992. The dilemma of plants: to grow or defend. Quart. Rev. Biol. 67: 283–335.CrossRefGoogle Scholar
  25. Heyworth, C. J., Iason, G. R., Temperton, V., Jarvis, P. G., and Duncan, A. J. 1998. The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L. Oecologia 115:344–350.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Joe, S. M., and Daheler, C. C. 2008. Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian islands. Biol. Invasions 10:245–255.CrossRefGoogle Scholar
  28. Johnson, R. H., Hull-sanders, H. M., and Meyer, G. A. 2007. Comparison of foliar terpenes between native and invasive Soliodago gigantean. Biochem. Syst. Ecol. 35:821–830.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. Kainulainen, P., Okanen, J., Palomäki, V., Holopainen, J. K., and Holipainen, T. 1991. Effect of drought and waterlogging stress on needle monoterpene of Picea abies. Can. J. Bot. 70:1613–1616.Google Scholar
  31. Kainulainen, P., Holopainen, J., Palomäki, V., and Holopainen, T. 1996. Effects of nitrogen fertilization on secondary chemistry and ectomycorrhizal state of Scots pine seedlings and on growth of grey pine aphid. J. Chem. Ecol. 22:617–636.CrossRefGoogle Scholar
  32. Kainulainen, P., Utriainen, J., Holopainen, J. K., Oksanen, J., and Holopainen, T..2000. Influence of elevated ozone and limited nitrogen availability on conifer seedlings in an open-air fumigation system: effects on growth, nutrient content, mycorrhizae, needle ultrastructure, starch and secondary compounds. Global Change Biol. 6:345–355.CrossRefGoogle Scholar
  33. Kikuzaki, H., Sato, A., Mayahara, Y., and Nakatani, N. 2000. Gallolyglucosides from berries of Pimenta dioica. J. Nat. Products 63:749–752.CrossRefGoogle Scholar
  34. Komai, K., and Tang, C. S. 1989 Chemical constituents and inhibitory activities of essential oils from Cyperus brevifolius and C. Kyllingia. J. Chem. Ecol. 15:2171–2176.CrossRefGoogle Scholar
  35. Lavin, S. R., Karasov, W. H., Ives, A. R., Middleton, 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.CrossRefPubMedGoogle Scholar
  36. Lee, K. D., Yang, M. S., Supanjani, and Smith, D. L. 2005. Fertilizer effect on the yield and terpene components from the flowerheads of Chrysanthemum boreale M. (Compositae). Agron. Sustain. Dev. 25:205–211.Google Scholar
  37. 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.CrossRefGoogle Scholar
  38. Llusià, J., and PEñuelas, J. 1998. Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Can. J. Bot. 76:1366–1373.CrossRefGoogle Scholar
  39. Llusià, J., and Peñuelas, J. 2001. Emission of volatile organic compounds by apple trees under spider mite attack and attraction of predatory mites. Exper. Appl. Acarol. 25:67–77.Google Scholar
  40. Llusià, J., Peñuelas, J., Asensio, D., and Munne-bosch, S. 2005. Airborne limonene confers limited thermobalance to Quercus ilex. Physiol. Plantarum 123: 40–48.CrossRefGoogle Scholar
  41. Loomis, W. E. 1932. Growth–differentiation balance vs. carbohydrate–nitrogen ratio. Proc. Am. Soc. Hortic. Sci. 29: 240–245.Google Scholar
  42. Loreto, F., and Velikova, V. 2001. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol. 127:1781–1787.CrossRefPubMedGoogle Scholar
  43. Loreto, F., Pinelli, P., Manes, F., and Kollist, H. 2004. Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol. 24:361–367.PubMedGoogle Scholar
  44. Mack, M. C., and D’anatonio, C. M. 2003. Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol. Appl. 13:154–166.Google Scholar
  45. Malowicki, S. M. M., Martin, R., and Qian, M. C. 2008. Volatile composition in raspberry cultivars grown in the Pacific northwest determined by stir bar sorptive extraction-gas chromatography-mass spectrometry. J. Agricul. Food Chem. 56: 4128–4133.CrossRefGoogle Scholar
  46. Maron, J. L, Vilà, M., Bommarco, R., Elmendorf, S., and Beardsley, P. 2004. Rapid evolution of invasive plants. Ecol. Monogr. 74:261–280.CrossRefGoogle Scholar
  47. Mooney, H. A., and Hobbs, R. J. 2000. Invasive Species in a Changing World. Island Press. Washington. US. p. 457.Google Scholar
  48. Moore, B. D., Wallis, I. R., Pala-paúl, J., Brophy, J. J., Willis, R. H., and Foley, W. J. 2004. Antiherbivore chemistry of Eucalyptus- cues and deterrents for marsupial folivores. J. Chem. Ecol. 30:1743–1769.CrossRefPubMedGoogle Scholar
  49. Múller-dombois, D., and Fosberg, F. R. 1998. Vegetation of the Tropical Pacific Islands. Spring Verlag, New York.Google Scholar
  50. Múller-schárer, H., Schaffner, U., and Steinger, T. 2004. Evolution in invasive plants: implications for biological control. Trends Ecol. Evol. 19:417–422.CrossRefPubMedGoogle Scholar
  51. Munné-bosch, S., Peñuelas, J., Asensio, D., and Llusià, J. 2004. Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. Plant Physiol. 136:2937–2947.CrossRefPubMedGoogle Scholar
  52. Ogunkova, L. Olubajo, O. O., and Sondha, D. S. 1972. Triterpenoid alcohols from Trema orientalis. Phytochem. Rep. 11:3093–3094.CrossRefGoogle Scholar
  53. Olajide, O. A., Awe, S. O., and Makinde, J. M. 1999. Pharmacological studies on the leaf of Psidium guajava. Fitoterapia 70:25–31.CrossRefGoogle Scholar
  54. Pachanawan, A., Phumkhachorn, P., and Rattanachaikunsopon, P. 2008. Potential of Psidium guajava supplemented fish diets in controlling Aeromonas hydrophila infection in Tilapia (Oreochromis niloticus). J. Biosci. Bioeng. 106:419–424.CrossRefPubMedGoogle Scholar
  55. Peñuelas, J., and Estiarte, M. 1998. Can elevated CO2 affect secondary metabolism and ecosystem functioning? Trends Ecol. Evol. 13: 20–24.CrossRefGoogle Scholar
  56. Peñuelas, J., and Llusià, J. 2001. The complexity of factors driving volatile organic compound emissions by plants. Biol. Plantarum 44:481–487.CrossRefGoogle Scholar
  57. Peñuelas, J., and Llusià, J. 2002. Linking photorespiration, monoterpenes and thermotolerance in Quercus. New Phytol. 155:227–237.CrossRefGoogle Scholar
  58. Peñuelas, J., and Llusià, J. 2003. BVOCs: Plant defense against climate warming? Trends Plant Sci. 8:105–109.CrossRefPubMedGoogle Scholar
  59. Peñuelas, J., and Llusià, J. 2004. Plant VOC emissions: making use of the unavoidable. Trends Ecol. Evol. 19:402404.CrossRefPubMedGoogle Scholar
  60. Peñuelas, J., and Munné-bosch, S. 2005. Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci. 10:166–169.CrossRefPubMedGoogle Scholar
  61. Peñuelas, J., Llusià, J., and Estiarte, M. 1995. Terpenoids: a plant language. Trends Ecol. Evol. 10:289.CrossRefGoogle Scholar
  62. Peñuelas, J., Llusià, J. Asensio, D., and Munné-bosch, S. 2005. Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ. 28: 278–286.CrossRefGoogle Scholar
  63. Peñuelas, J., Sardans, J., Llusià, J., Owen, S., Carnicer, J., Giambelluca, T. W., Rezende, E. L., Waite, M., and Niinemets, Ü. 2009. Faster returns on ‘leaf economics’, and different biochemical niche in plant invasive than in native species. Global Change Biol. doi:10.111/j.1365-2486.2009.02054.x . Google Scholar
  64. 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.CrossRefGoogle Scholar
  65. Pino, J. A., Mesa, J., Muñoz, Y., Martí, M. P., and Marbot, R. 2005. Volatile components from Mango (Mangifera indica L.) cultivars. J. Agric. Food Chem. 53:2213–2223.CrossRefPubMedGoogle Scholar
  66. Porder, S., Sner, G. P., and Vitousek, P. M. 2005. Ground-based and remotely sensed nutrient availability across a tropical landscape. Proc. Nat. Acad. Sci. USA 102:10909–10912.CrossRefPubMedGoogle Scholar
  67. Randrianalijaona, J. A., Ramanoelipa, P. A. R., Rasoarahona, J. R. E., and Gaydou, E. M. 2005. Seasonal and chemotype influences on the chemical composition of Lantana camara L. essential oils from Madagascar. Anal. Chim. Acta 545:46–52.CrossRefGoogle Scholar
  68. Reich, P. B., Walters, M. B., and Ellsworth, D. S. 1997. From tropics to Tundra: global convergence in plant functioning. Proc. Nat. Acad. Sci. USA 94:13730–13734.CrossRefPubMedGoogle Scholar
  69. Rogers, W. E., Siemann, E. 2004. Invasive ecotypes tolerate herbivory more effectively than native ecotypes of the Chinese tallow tree Sapium sebiferum. J. Appl. Ecol. 41:561–570.CrossRefGoogle Scholar
  70. Schapoval, E. E. S., Winter de bargas, M. R., Chaves, C. G., Bridi, R., Zuanazzi, J. A., and Henriqurs, A. T. 1998. Anti-inflammatory and anticonceptive activities of extracts and isolated compounds from Stachytarpheta cayennensis. J. Ethnopharmacol. 60:53–59.CrossRefPubMedGoogle Scholar
  71. Sharkey, T. D., and Singsaas, E. L. 1995. Why plants emit isoprene. Nature 374:769.CrossRefGoogle Scholar
  72. Sharma, O. P., Maklar, H. P. S., and Dawra, R. K. 1999. A review of the noxious plant Lantana camara. Toxicon 26:975–987.CrossRefGoogle Scholar
  73. Siemann, E., Rogers, W. E., and Dewalt, S. J. 2006. Rapid adaptation of insect herbivores to an invasive plant. Proc. R. Soc. B 273:2763–2769.CrossRefPubMedGoogle Scholar
  74. Son, Y., Kim, Z. S., Hwang, J. H., and Park, J. S. 1998. Fertilization effects on growth, foliar nutrients and extract concentration in Ginkgo seedlings. J. Korean For. Soc. 87:98–105.Google Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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.Google Scholar
  77. Vitousek, P. M., and Walker, L. R. 1989. Biological invasion by Myrica Faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol. Monographs 59:247–265.CrossRefGoogle Scholar
  78. 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.Google Scholar
  79. Webb, C. O., and Donoghue, M. J. 2005. Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5:181–183.CrossRefGoogle Scholar
  80. Wheeler, G. S., Massey, L. M., and Southwell, I. A. (2002) Antipredator defense of biological control agent Oxyops vitiosa is mediated by plant volatiles sequesters from the host plant. J. Chem. Ecol. 28:297–315.CrossRefPubMedGoogle Scholar
  81. 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, M., Garnier, J., Groom, E., Gulias, P. K., Hikosaka, J., Lamont, K., Lee, B. B., Lee, T., Lusk, W., Midgley, C., Navas, J. J., Niinemets, M. L., Oleksyn, Ü., Osada, J., Porter, N., Poot,, H., Prior, L., Pyankov, V. I., Roumet, C., Thomas, S. C., Tjoelker, M. G., Veneklaas, E. J., and Villar, R. 2004. The worldwide leaf economics spectrum. Nature 428:821–827.CrossRefPubMedGoogle Scholar
  82. Yang, T., Li, J., Wang, H. X., and Zeng, Y. 2005. A gerantiol-synthase gene from Cinnamomum tenuipilum. Phytochemistry 66:285–293.CrossRefPubMedGoogle Scholar
  83. Zhao, X., Zhang, G. W., Niu, X. M., Li, W. Q., Wang, F. S., and Li, S. H. 2009. Terpenes from Eupatorium adenophorum and their allelopathic effects on Arabidopsis seeds germination. J. Agricul. Food Chem. 57:478–482.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Jordi Sardans
    • 1
    Email author
  • Joan Llusià
    • 1
  • Ülo Niinemets
    • 3
  • Sue Owen
    • 2
  • Josep Peñuelas
    • 1
  1. 1.Global Ecology Unit CSIC-CEAB-CREAF, Facultat de Ciencies, Edifici CUniversitat Autònoma de BarcelonaBellaterraSpain
  2. 2.Centre for Ecology and Hydrology EdinburghScotlandGreat Britain
  3. 3.Estonian University of Life Sciences, Institute of Agricultural and Environmental SciencesTartuEstonia

Personalised recommendations