A screening study of leaf terpene emissions of 43 rainforest species in Danum Valley Conservation Area (Borneo) and their relationships with chemical and morphological leaf traits

Plant Biosystems

Volumn 148, Issue 2, 2014, Pages 307-317

  Llusia, Joan ^a,b   Sardans, Jordi ^a,b   Niinemets, Ülo ^c   Owen, Susan M ^d   Peñuelas, Josep ^a,b  

^a CREAF   (Spain)

^b CSIC   (Spain)

^c ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^d CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Herbivory; LMA; nitrogen; phosphorus; terpene emissions; trace elements

Indexed keywords

EID: 84898860373     PISSN: 11263504     EISSN: 17245575     Source Type: Journal    
DOI: 10.1080/11263504.2013.770803     Document Type: Article

References (88)

1. BanchioE, ZygadloY, ValladaresGR. 2005. Effects of mechanical wounding on essential oil composition and emission of volatiles from Minthostachys mollis. J Chem Ecol31: 719-727.
2. BlanchJS, PeñuelasJ, LlusiaJ. 2007. Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. Physiol Plantarum131: 211-225.
3. BlombergSP, GarlandT, IvesAR. 2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution57: 717-745.
4. BlombergSP, GarlandT. 2002. Tempo and mode in evolution: Phylogenetic inertia, adaptation and comparative methods. J Evol Biol15: 899-910.
5. BohlmannJ, Meyer-GauenG, CroteauR. 1998. Plant terpenoid synthases: Molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA95: 4126-4133.
6. BrasseurGP, OrlandoJJ, TyndallGS. 1999. Atmospheric chemistry and global change. New York: Oxford University Press.
7. BrearleyFQ, ScholesJD, PressMC, PalfnerG. 2007. How does light and phosphorus fertilisation affect the growth and ectomycorrhizal community of two contrasting dipterocarp species?Plant Ecol192: 237-249.
8. BryantJP, ChapinFS, KleinDR. 1983. Carbon nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos40: 357-368.
9. ChameidesWL, LindsayRW, RichardsonJ, KiangCS. 1988. The role of biogenic hydrocarbons in urban photochemical smog - Atlanta as a case-study. Science241: 1473-1475.
10. CopoloviciLO, FilellaI, LlusiaJ, NiinemetsU, PeñuelasJ. 2005. The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol139: 485-496.
11. CornaraL, BononiM, TateoE, Serrato-ValentiG, MariottiMG. 2001. Trichomes on vegetative and reproductive organs of Stevia rebaudiana (Asteraceae). Structure and secretory products. Plant Biosyst135: 25-37.
12. CronnDR, NutmagulW. 1982. Analysis of atmospheric hydrocarbons during winter Monex. Tellus34: 159-165.
13. DickeM, SabelisMW, TakabayashiJ. 1991. Do plants cry for help - Evidence related to a tritrophic system of predatory mites, spider-mites and their host plants. Insects-Plants89(39): 127-134.
14. FaresS, BrilliF, NoguesI, VelikovaV, TsonevT, DagliS, et al. 2008. Isoprene emission and primary metabolism in Phragmites australis grown under different phosphorus levels. Plant Biol10: 38-43.
15. FehsenfeldF, CalvertJ, FallR, GoldanP, GuentherAB, HewittCN, et al. 1992. Emissions of volatile organic compounds from vegetation and the implications for atmospheric chemistry. Global Biogeochem Cy6: 389-430.
16. FunkJL, JonesCG, LerdauMT. 1999. Defoliation effects on isoprene emission from Populus deltoides. Oecologia118: 333-339.
17. GarlandTJ, HarveyPH, IvesAR. 1993. Procedures for the analysis of comparative data using phylogenetically independent contrast. Syst Biol41: 18-32.
18. GolsR, BullockJM, DickeM, BukovinszkyT, HarveyJA. 2011. Smelling the wood from the trees: Non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage. J Chem Ecol37: 795-807.
19. GuentherA, ZimmermanP, WildermuthM. 1994. Natural volatile organic-compound emission rate estimates for United-States Woodland Landscapes. Atmos Environ28: 1197-1210.
20. HarleyPC, LitvakME, SharkeyTD, MonsonRK. 1994. Isoprene emission from velvet bean-leaves - Interactions among nitrogen availability, growth photon flux-density, and leaf development. Plant Physiol105: 279-285.
21. HarmelN, AlmohamadR, FauconnierML, Du JardinP, VerheggenF, MarlierM, et al. 2007. Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus. Insect Sci14: 57-63.
22. HermsDA, MattsonWJ. 1992. The dilemma of plants - To grow or defend. Q Rev Biol67: 283-335.
23. HewittCN, AshworthK, BoynardA, GuentherA, LangfordB, MacKenzieAR, et al. 2011. Ground-level ozone influenced by circadian control of isoprene emissions. Nat Geosci4: 671-674.
24. HewittCN, MacKenzieAR, Di CarloP, Di MarcoCF, DorseyJR, EvansM, et al. 2009. Nitrogen management is essential to prevent tropical oil palm plantations from causing ground-level ozone pollution. Proc Natl Acad Sci USA106: 18447-18451.
25. KainulainenP, OksanenJ, PalomakiV, HolopainenJK, HolopainenT. 1992. Effect of drought and waterlogging stress on needle monoterpenes of Picea abies. Can J Bot70: 1613-1616.
26. KaligaricM, MeisterMH, SkornikS, SajnaN, KrambergerB, Bolhar-NordenkampfHR. 2011. Grassland succession is mediated by umbelliferous colonizers showing allelopathic potential. Plant Biosyst145: 688-698.
27. KingDJ, GleadowRM, WoodrowIE. 2004. Terpene deployment in Eucalyptus polybractea: Relationships with leaf structure, environmental stresses, and growth. Funct Plant Biol31: 451-460.
28. KitayamaK, AlbaSI, Majalab-LeeN, OhsawaM. 2002. Soil nitrogen mineralization rates of rainforest in a matrix of elevations and geological substrates on Mount Kinabalu (Borneo). Ecol Res13: 301-312.
29. KitayamaK, Majalap-LeeN, AibaS. 2000. Soil phosphorus fractionation and phosphorus-use efficiencies of tropical rainforests along altitudinal gradients of Mount Kinabalu. Borneo. Oecologia123: 342-349.
30. KlingerLF, LiQJ, GuentherAB, GreenbergJP, BakerB, BaiJH. 2002. Assessment of volatile organic compound emissions from ecosystems of China. J Geophys Res Atmos: 107.
31. KnudsenJT, ErikssonR, GershenzonJ, StahlB. 2006. Diversity and distribution of floral scent. Bot Rev72: 1-120.
32. KurokawaH, KitahashiY, KoikeT, LaiJ, NakashizukaT. 2004. Allocation to defense or growth in dipterocarp forest seedlings in Borneo. Oecologia140: 261-270, doi: 10.1007/s00442-004-1566-7.
33. LavinSR, KarasovWH, IvesAR, MiddletonKM, GarlandT. 2008. Morphometrics of the avian small intestine compared with that of nonflying mammals: A phylogenetic approach. Physiol Biochem Zoolog81: 526-550.
34. LitvakME, LoretoF, HarleyPC, SharkeyTD, MonsonRK. 1996. The response of isoprene emission rate and photosynthetic rate to photon flux and nitrogen supply in aspen and white oak trees. Plant Cell Environ19: 549-559.
35. LlusiaJ, PeñuelasJ, AsensioD, Munne-BoschS. 2005. Airborne limonene confers limited thermotolerance to Quercus ilex. Physiol Plantarum123: 40-48.
36. LlusiaJ, PeñuelasJ, SardansJ, OwenSM, NiinemetsU. 2010. Measurement of volatile terpene emissions in 70 dominant vascular plant species in Hawaïi: Aliens emit more than natives. Global Ecol Biogeogr19: 863-874.
37. LlusiaJ, PeñuelasJ. 1998. Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Can J Bot76: 1366-1373.
38. LlusiaJ, PeñuelasJ. 2001. Emission of volatile organic compounds by apple trees under spider mite attack and attraction of predatory mites. Exp Appl Acarol25: 65-77.
39. LoomisWE. 1932. Growth-differentiation balance vs. carbohydrate-nitrogen ratio. Proc Am Soc Hortic Sci29: 240-245.
40. LoretoF, PinelliP, ManesF, KollistH. 2004. Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol24: 361-367.
41. LoretoF, VelikovaV. 2001. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol127: 1781-1787.
42. MakkarHPS, GoodchildAV. 1996. Quantification of tannins: A laboratory manual. Aleppo: International Center for Agricultural Research in the Dry Areas (ICARDA).
43. MarigoG. 1973. Sur une méthode de fractionnement et d'estimation de composes phénoliques chez les végétaux. Analusis2: 106-110.
44. MisztalPK, OwenSM, GuentherAB, RasmussenR, GeronC, HarleyP, et al. 2010. Large estragole fluxes from oil palms in Borneo. Atmos Chem Phys10: 4343-4358.
45. MummR, HilkerM. 2006. Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci11: 351-358.
46. Munne-BoschS, PeñuelasJ, AsensioD, LlusiaJ. 2004. Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. Plant Physiol136: 2937-2947.
47. NiinemetsU, ArnethA, KuhnU, MonsonRK, PeñuelasJ, StaudtM. 2010. The emission factor of volatile isoprenoids: Stress, acclimation, and developmental responses. Biogeosciences7: 2203-2223.
48. NiinemetsU, ValladaresF, CeulemansR. 2003. Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant Cell Environ26: 941-956.
49. NomuraN, KikuzawaK. 2003. Productive phenology of tropical montane forests: Fertilization experiments along a moisture gradient. Ecol Res18: 573-586.
50. OpitzS, KunertG, GershenzonJ. 2008. Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol34: 508-522.
51. OrmenoE, FernandezC, Bousquet-MelouA, GreffS, MorinE, RoblesC, et al. 2007. Monoterpene and sesquiterpene emissions of three Mediterranean species through calcareous and siliceous soils in natural conditions. Atmos Environ41: 629-639.
52. OrmeñoE, FernandezC. 2012. Effect of soil nutrient on production and diversity of volatile terpenoids from plants. Curr Bioact Comp8: 71-79.
53. OwenS, BoissardC, StreetRA, DuckhamSC, CsikyO, HewittCN. 1997. Screening of 18 Mediterranean plant species for volatile organic compound emissions. Atmos Environ31: 101-117.
54. OwenSM, BoissardC, HewittCN. 2001. Volatile organic compounds (VOCs) emitted from 40 Mediterranean plant species: VOC speciation and extrapolation to habitat scale. Atmos Environ35: 5393-5409.
55. OwenSM, PeñuelasJ. 2005. Opportunistic emissions of volatile isoprenoids. Trends Plant Sci10: 420-426.
56. PadhyPK, VarshneyCK. 2005. Emission of volatile organic compounds (VOC) from tropical plant species in India. Chemosphere59: 1643-1653.
57. PaoliGD, CurranLM, ZakDR. 2005. Phosphorus efficiency of Bornean rain forest productivity: Evidence against the unimodal efficiency hypothesis. Ecology86: 1548-1561.
58. PaoliGD. 2006. Divergent leaf traits among congeneric tropical trees with contrasting habitat associations on Borneo. J Trop Ecol22: 397-408.
59. PeñuelasJ, EstiarteM. 1998. Can elevated CO2 affect secondary metabolism and ecosystem function?Tree13: 20-24.
60. PeñuelasJ, LlusiaJ, AsensioD, Munne-BoschS. 2005. Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ28: 278-286.
61. PeñuelasJ, LlusiaJ. 2001. The complexity of factors driving volatile organic compound emissions by plants. Biol Plantarum44: 481-487.
62. PeñuelasJ, LlusiaJ. 2002. Linking photorespiration, monoterpenes and thermotolerance in Quercus. New Phytol155: 227-237.
63. PeñuelasJ, LlusiaJ. 2003. BVOCs: Plant defense against climate warming?Trends Plant Sci8: 105-109.
64. PeñuelasJ, LlusiaJ. 2004. Plant VOC emissions: Making use of the unavoidable. TREE19: 402-404.
65. PeñuelasJ, Munne-BoschS. 2005. Isoprenoids: An evolutionary pool for photoprotection. Trends Plant Sci10: 166-169.
66. PeñuelasJ, RibasM, GonzalezM, Azcón-BietoJ. 1994. Water status, photosynthetic pigments, C/N ratios and respiration rates of Sitka spruce seedlings exposed to 70 ppbv ozone for a summer. Environ Exp Bot34: 443-449.
67. PeñuelasJ, SardansJ, LlusiaJ, OwenSM, NiinemetsÜ. 2011. Lower P contents and more widespread terpene presence in old Bornean than in young Hawaiian tropical plants species guilds. Ecosphere2(45): 1-19.
68. PeñuelasJ, SardansJ, LlusiaOwenS, CarnicerJ, GiambellucaTW, RezendeEL, et al. 2010. Faster returns on "leaf economics" and different biogeochemical niche in invasive compared with native plant species. Global Change Biol16: 2171-2185.
69. PeñuelasJ, StaudtM. 2010. BVOCs and global change. Trends Plant Sci15: 133-144.
70. PeñuelasJ, SardansJ, LlusiaJ, SilvaJ, OwenSM, Bala-OlaB, et al. 2013. Foliar chemistry and standing folivory of early and late successional species in a Bornean rainforest. Plant Ecol Divers, In Press, doi: 10.1080/17550874.2013.768713.
71. PiesikD, PankaD, DelaneyKJ, SkoczekA, LamparskiR, WeaverDK. 2011. Cereal crop volatile organic compound induction after mechanical injury, beetle herbivory (Oulema spp.), or fungal infection (Fusarium spp.). J Plant Physiol168: 878-886.
72. PorterLJ, HrstichLN, ChangBG. 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry25: 223-230.
73. RaghavaT, RavikumarP, HegdeR, KushA. 2010. Spatial and temporal volatile organic compound response of select tomato cultivars to herbivory and mechanical injury. Plant Sci179: 520-526.
74. SampedroL, MoreiraX, LlusiaJ, PeñuelasJ, ZasR. 2010. Genetics, phosphorus availability, and herbivore-derived induction as sources of phenotypic variation of leaf volatile terpenes in a pine species. J Exp Bot61: 4437-4447.
75. SardansJ, LlusiaJ, OwenSM, NiinemetsÜ, PeñuelasJ. 2013. Screening study of leaf terpene concentration of 75 Borneo rainforest plant species: Relationships with leaf elemental concentrations and morphology. Rec Nat Prod., In Press.
76. SharkeyTD, SingsaasEL. 1995. Why plants emit isoprene. Nature374: 769.
77. SinghAP, SinghR, MinaU, SinghMP, VarshneyChK. 2011. Emissions of monoterpene from tropical Indian plant species and assessment of VOC emission from the forest of Haryana state. Atmos Pollut Resdoi: 10.5094/APR.2011.009 2: 72-79.
78. SingletonVL, RossiJA. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic16: 144-158.
79. SoepadmoE, ShawLG, ChungRCK. 2004. Tree flora of Sabah and Sarawak. Koala Lumpur: Sabah Forestry Department, Malaysia, Forest Research Institute.
80. SteidleJLM, van LoonJJA. 2003. Dietary specialization and infochemical use in carnivorous arthropods: Testing a concept. Entomol Exp Appl108: 133-148.
81. ThompsonAM. 1992. The oxidizing capacity of the earths atmosphere - Probable past and future changes. Science256: 1157-1165.
82. TrainerM, WilliamsEJ, ParrishDD, BuhrMP, AllwineEJ, WestbergHH, et al. 1987. Models and observations of the impact of natural hydrocarbons on rural ozone. Nature329: 705-707.
83. VetLEM, DickeM. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol37: 141-172.
84. WangM, LincolnDE. 2004. Effects of light intensity and artificial wounding on monoterpene production in Myrica cerifera from two different ecological habitats. Can J Bot82: 1501-1508.
85. WelterS, Bracho-NunezA, MirC, ZimmerI, KesselmeierJ, LumaretR, et al. 2012. The diversification of terpene emissions in Mediterranean oaks: Lessons from a study of Quercus suber, Quercus canariensis and its hybrid Quercus afares. Tree Physiol32: 1082-1091.
86. WheelerGS, MasseyLM, SouthwellIA. 2002. Antipredator defense of biological control agent Oxyops vitiosa is mediated by plant volatiles sequestered from the host plant Melaleuca quinquenervia. J Chem Ecol28: 297-315.
87. WhitmoreTC. 1972. Tree flora of Malaya. A manual for foresters. Koala Lumpur: Longman Malaysia.
88. ZhangYF, XieYP, XueJL, PengGL, WangX. 2009. Effect of volatile emissions, especially alpha-pinene, from persimmon trees infested by Japanese wax scales or treated with methyl jasmonate on recruitment of ladybeetle predators. Environ Entomol38: 1439-1445.