Foliar Mono- and Sesquiterpene Contents in Relation to Leaf Economic Spectrum in Native and Alien Species in Oahu (Hawai’i) Jordi Sardans & Joan Llusià & Ülo Niinemets & Sue Owen & Josep Peñuelas Received: 18 November 2009 / Revised: 03 January 2010 / Accepted: 5 January 2010 / Published online: 11 February 2010 # Springer Science+Business Media, LLC 2010 Abstract 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 μgg −1 ) than native species (830±227 μgg −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. Keywords Hawaiian Islands . Terpene content . Nitrogen . Phosphorus . Alien species . Native species . LMA . Photosynthetic capacity . Monoterpenes . Sesquiterpenes . Nutrient driven hypothesis . “Excess carbon” hypothesis . Modified EICA hypothesis Introduction Plant invasion is an important component of current global change (Mooney and Hobbs 2000). Chemical factors such as terpenes can be involved in the competition between alien and native plant species. For example, Barney et al. (2005) stated that the terpene production capacity of Artemisia vulgaris can be a key factor in its establishment and proliferation in introduced habitats by phytotoxic effects on native species. Many studies have investigated the physiological and ecological significance of terpenes in plants. Protection, defense, and infochemical function have been highlighted as roles of terpenes (Llusià and Peñuelas 2001; Wheeler et al. 2002; Peñuelas and Llusià 2003, 2004). Examples of these roles are photoprotection (Peñuelas and Munné-Bosch 2005), thermotolerance (Sharkey and Singsaas 1995; Peñuelas and Llusià 2001, 2002; Copolovici et al. 2005; Peñuelas et al. 2005), protection against drought stress J. Sardans (*) : J. Llusià : J. Peñuelas Global Ecology Unit CSIC-CEAB-CREAF, Facultat de Ciencies, Edifici C, Universitat Autònoma de Barcelona, 08913 Bellaterra, Spain e-mail: [email protected]S. Owen Centre for Ecology and Hydrology Edinburgh, Bush Estate, Penicuik, EH26 0QB Scotland, Great Britain Ü. Niinemets Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Kreutzwaldi 1, 51014 Tartu, Estonia J Chem Ecol (2010) 36:210–226 DOI 10.1007/s10886-010-9744-z
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Foliar Mono- and Sesquiterpene Contents in Relation to LeafEconomic Spectrum in Native and Alien Speciesin Oahu (Hawai’i)
Jordi Sardans & Joan Llusià & Ülo Niinemets &
Sue Owen & Josep Peñuelas
Received: 18 November 2009 /Revised: 03 January 2010 /Accepted: 5 January 2010 /Published online: 11 February 2010# Springer Science+Business Media, LLC 2010
Abstract Capacity for terpene production may conferadvantage in protection against abiotic stresses such as heatand drought, and also against herbivore and pathogenattack. Plant invasive success has been intense in theHawaiian islands, but little is known about terpene contentin native and alien plant species on these islands. Weconducted a screening of leaf terpene concentrations in 35native and 38 alien dominant plant species on Oahu island.Ten (29%) of the 35 native species and 15 (39%) of the 38alien species contained terpenes in the leaves. This is thefirst report of terpene content for the ten native species, and for10 of the 15 alien species. A total of 156 different terpenes (54monoterpenes and 102 sesquiterpenes) were detected. Terpenecontent had no phylogenetic significance among the studiedspecies. Alien species contained significantly more terpenes inleaves (average ± SE=1965±367 μg g−1) than native species(830±227 μg g−1). Alien species showed significantly higherphotosynthetic capacity, N content, and lower Leaf MassArea (LMA) than native species, and showed higher totalterpene 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 wereconsistent with the “nutrient driven synthesis” hypothesis.Comparing alien and native species, the results also supportthe modified Evolution of Increased Competitive Ability(EICA) hypothesis that suggests that alien success may befavored by a defense system based on an increase inconcentrations of less costly defenses (terpenes) againstgeneralist herbivores.
Plant invasion is an important component of current globalchange (Mooney and Hobbs 2000). Chemical factors suchas terpenes can be involved in the competition betweenalien and native plant species. For example, Barney et al.(2005) stated that the terpene production capacity ofArtemisia vulgaris can be a key factor in its establishmentand proliferation in introduced habitats by phytotoxiceffects on native species.
Many studies have investigated the physiological andecological significance of terpenes in plants. Protection,defense, and infochemical function have been highlightedas roles of terpenes (Llusià and Peñuelas 2001; Wheeler etal. 2002; Peñuelas and Llusià 2003, 2004). Examples ofthese roles are photoprotection (Peñuelas and Munné-Bosch2005), thermotolerance (Sharkey and Singsaas 1995;Peñuelas and Llusià 2001, 2002; Copolovici et al. 2005;Peñuelas et al. 2005), protection against drought stress
J. Sardans (*) : J. Llusià : J. PeñuelasGlobal Ecology Unit CSIC-CEAB-CREAF, Facultat de Ciencies,Edifici C, Universitat Autònoma de Barcelona,08913 Bellaterra, Spaine-mail: [email protected]
S. OwenCentre for Ecology and Hydrology Edinburgh,Bush Estate, Penicuik,EH26 0QB Scotland, Great Britain
Ü. NiinemetsEstonian University of Life Sciences,Institute of Agricultural and Environmental Sciences,Kreutzwaldi 1,51014 Tartu, Estonia
(Llusià and Peñuelas 1998; Kainulainen et al. 1991), andnon-specific antioxidative capacity, whereby terpenes pro-tect photosynthetic membranes against peroxidation andreactive oxygen species such as singlet oxygen (Loreto andVelikova 2001; Peñuelas and Llusià 2002; Loreto et al.2004; Munné-Bosch et al. 2004; Llusià et al. 2005).
Although relative performance often depends on growthconditions, invaders are more likely to have higher leaf areaand lower tissue construction costs that increase productivity,and also greater phenotypic plasticity that is advantageous indisturbed environments (Daehler 2005). Foliar traits such ashigher photosynthetic capacity per dry mass (Amass) andlower leaf construction costs associated with a lower leafmass per area (LMA) partly explain the success of alien plantspecies (Baruch and Goldstein 1999; Funk and Vitousek2007), since they may contribute to faster growth rates forinvaders and confer a competitive advantage over nativespecies (Reich et al. 1997; Peñuelas et al. 2010). Similarly,invasive plant species in Hawai’i have been found to havehigher foliar N and P concentrations than native species(Peñuelas et al. 2010).
Changes in nutrient availability can affect terpeneproduction (Son et al. 1998; Kainulainen et al. 2000; Leeet al. 2005). Greater terpene production in plants withhigher nutrient concentration and photosynthetic rates canbe expected from the “nutrient-driven synthesis” hypothesisthat predicts a larger enzyme production with greatercellular N and P availability. Higher nutrient availabilityusually is expected to translate into higher carbon fixationand activity of the enzymes involved in isoprenoidproduction (Harley et al. 1994; Litvak et al. 1996). Incontrast, a lower production of terpenes as carbon basedsecondary compounds under higher nutrient availabilities canbe expected from the “carbon based secondary compounds”(CBSC) hypthesis and the source-sink “carbon-nutrientbalance” or “excess carbon” (CNB) hypothesis (Loomis1932; Bryant et al. 1983; Herms and Mattson 1992; Peñuelasand Estiarte 1998). These hypotheses assert that plantsallocate carbon to secondary metabolism only after growthrequirements are met, and that growth is constrained more bynutrients than by photosynthesis. According to these theories,the excess carbohydrates that accumulate in nutrient-limitedplants when photosynthesis outpaces growth are diverted tothe production of carbon-based secondary compounds (e.g.,terpenes and phenolics).
Phenotypic plasticity has been an important mechanismthat enables alien plants to colonize exotic habitats, andrecent studies indicate that alien plants also can evolvequickly (Maron et al. 2004). Some invasive trees and herbshave proved to be able to evolve in periods from 1 to 3hundred years or less, reaching a faster growth capacity,and changing their chemical defense strategies (Rogers andSiemann 2004; Siemann et al. 2006). The main cause of
this increase in fitness has been proposed as the Evolution ofIncreased Competitive Ability (EICA) hypothesis (Blosseyand Nötzold 1995). It predicts that introduced species, whichlose contact with their natural specialist herbivores, mayevolve, thus decreasing their investment in anti-herbivorechemical defenses. This way, resources no longer needed fordefense can be reallocated to other functions that provide aselective advantage in the novel habitat. Recent modifica-tions in the development of increased competitive ability(EICA) hypothesis propose that since invasive genotypesstill may experience attack by local generalist herbivores(Müller-Schärer et al. 2004), selection may favor a reductionin the expression of metabolically expensive chemicaldefenses effective against specialist herbivores, and increasethe concentrations of less costly qualitative defenses, such asterpenes, that may be more toxic to generalist herbivores(Joshi and Vrieling 2005; Stastny et al. 2005). In this context,Johnson et al. (2007) have observed that when NorthAmerican native populations of Solidago gigantea growunder the same environment conditions as alien Europeanpopulation of the same species, the native plants have lowermonoterpene and diterpene contents than invasive plants.This suggests that terpene content might be related to aliensuccess.
The Hawaiian archipelago is the most isolated terrestrialregion on Earth (Vitousek and Walker 1989), and isespecially vulnerable to invasions by non indigenousspecies (Harrington and Ewel 1997). Alien plants inHawai’i have strong impact on native Hawaiian ecosystemsand their highly endemic flora (Mack and D’Antonio 2003;Hughes and Uowolo 2006). In these Islands, around 861flowering plant species (47% of total Hawaiian angiospermflora) are naturalized alien species (Wagner et al. 1999). Asa result, approximately 25% of the Hawaiian native flora,90% of which is endemic, has been listed as threatened orendangered. In fact, all tropical island ecosystems appear tobe especially vulnerable to invasive species, and someexperiments suggest that the high resource availability andthe poor ability of native species to capture these resources,contributes to the vulnerability of island communities to theestablishment and spread of alien species (Allison andVitousek 2004).
There are published reports of terpene contents inspecies that are aliens in Hawai’i, but these studies havebeen conducted in other parts of the world (Ogunkoya et al.1972; Schapoval et al. 1998; Kikuzaki et al. 2000; Wheeleret al. 2002; Chiang and Kuo 2002; Pino et al. 2005;Randrianalijaona, et al. 2005; Fernández and Torres 2006;Pachanawan et al. 2008). Generally, apart from scarcereports (Komai and Tang 1989) little is known aboutterpene content in Hawaiian native and alien flora.
In this study, we conducted a screening of leaf terpenecontent in 35 native and 38 alien dominant Hawaiian plant
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species. Our aims were to: (i) estimate terpene content andcomposition of native and alien species that are dominant inOahu, (ii) compare the mono- and sesquiterpene content of the35 native plants with the content of 38 alien plants, (iii)compare the relationships of terpene content with the leaftraits defining “leaf economics spectrum” (Wright et al. 2004),such as photosynthetic rates (Amass), leaf mass area (LMA),and C, N, P, and K leaf concentrations among native andalien species, and (iv) test the “nutrient driven synthesis”,“excess carbon”, and “modified EICA” hypotheses forterpene content in native and alien species.
Methods and Materials
Field Sites The study was conducted in May 2007 onOahu, the third largest of the Hawaiian Islands. As typicalof larger Hawaiian Islands, the climate is characterized bysteep rainfall gradients over short distances (Müller-Domboisand Fosberg 1998). Lowlands at the leeward side have apronounced dry summer season, while precipitation isdistributed almost uniformly in lowland and mountain rainforests. Due to the oceanic tropical climate, interannualtemperature oscillations are small with winters having onaverage 2–3°C cooler temperatures than summers. As largedifferences in the composition of native and alien vegetationoccur in response to rainfall gradients, four sites with distinctprecipitation regimes were selected for plant sampling in theleeward lowlands of Oahu, and at the leeward side of Koolaumountains (Table 1 and see detailed decription of thesampling sites, their climate and the studied species inPeñuelas et al. 2010).
The four key soil types found across the sites rankaccording to the state of soil weathering as oxisols>ultisols>mollisols>inceptisols (Uehara and Ikawa 2000; Deenik andMcClellan 2007).Mollisols exhibit the highest fertility, whilemore leached oxisols and ultisols with lower pH are amongthe soils with lowest fertility (Uehara and Ikawa 2000;Deenik and McClellan 2007). Inceptisols, the youngest soils,
typically show weak profile development, and, depending ongenesis, exhibit tremendous variability in fertility (Deenikand McClellan 2007). The Tantalus series inceptisols are ofmoderate to high fertility, while the inceptisols in rocky soilsand mountainous land are of low fertility. Thus, in our study,the broad soil classes rank according to fertility as mollisols> inceptisols (Tantalus) > oxisols ≅ ultisols > inceptisols(mountainous soils).
Study Species Altogether, 73 dominant,(35 native, and 38alien) species were studied at four sites (Peñuelas et al.2010). All native species sampled were evergreen, but indry sites (St. Louis Heights, Hahaione Valley), four alienspecies were drought-deciduous (Desmodium incanum,Falcataria moluccana, Senna surattensis, Tabebuia rosea),and two were semi-deciduous (Haematoxylum campechia-num, Leucaena leucocephala). The deciduous and semi-deciduous aliens were legumes, except for Tabebuia rosea(Bignoniaceae). Of the 73 studied species, 36 were trees, 29shrubs, 3 woody vines to shrubs, 3 woody vines, one herbto subshrub, and one parastitic mistletoe (Korthalsellacomplanata). The distribution of species among the keylife form classes was similar among native and alien species(14 alien and 15 native shrubs, 21 alien and 15 native trees;Peñuelas et al. 2010).
Each species was sampled in triplicate, with twigs orsmall branches taken from 3 individuals for each species.Samples were cut with a sharp knife and cut againimmediately with the excised stem under water, to preventingress of air to the xylem vessels and subsequent stress. Inthe lab, the excised stems were enclosed loosely in plasticbags to prevent water loss by transpiration prior to terpeneextraction. Leaf extractions were conducted during the next12 h. Species coordinates and sampling altitude were notedin each site by using GPS, and this information was used tolink species locations to specific soil types and to derivelocation-specific climatic data. Long-term average monthlyand annual precipitation, precipitation of the three driestmonths and annual precipitation, and average, maximum
Table 1 Description of the study sites
Site Coordinates Average ± SDa Average ± SD precipitation (mm) Average ± SD annual temperature (°C)
altitude (m) Annual Three driest months Minimum Maximum n N A
St. Louis Heights 21°18′N, 157°48′W 171±65 1430±210 197±45 18.7±0.5 26.9±0.5 12 0 12
N number of species, N native species, A alien speciesa averages are based on the number of species sampled and species-specific locations. In statistical analyses, exact species-specific environmentaldata were used
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and minimum temperatures were estimated from highresolution climatic grids by using the database developedand continuously updated by Giambelluca and associates(Giambelluca et al. 1986; Cao et al. 2007). ARCGIS 9.1was used to extrapolate between the isohyets (10 m squarecells in the grid with appropriate elevation model), asapplied previously in Hawaiian ecosystems (Porder et al.2005; Dunbar-Co et al. 2009).
Species were classified according to site preference asdry, dry-mesic, mesic, dry-wet, mesic-wet, and wet forestspecies. Species invasiveness was scored by using a four-level scale as 0 (native species), 1 (low invasiveness), 2(moderate-high), and 3 (very high). These simplified scoreswere based on the Australia/New Zealand weed riskassessment (WRA) system (Pheloung et al. 1999) modifiedto Hawai’i and other Pacific Islands (Daehler et al. 2004).For Hawaiian Islands, these scores are reported in PacificIsland Ecosystems at the Risk (PIER) project onlinedatabase, maintained by U.S. Forest Service’s Institute ofPacific Islands Forestry (http://www.hear.org/pier/), and onrecent updates on species invasive potential in Oahu(Daehler and Baker 2006). The weed risk assessment isbased on up to 49 questions about species biology. For 9species that have not been scored in these assessments, weedrisk assessment scores were derived based on the riskquestionnaire (http://www.hear.org/pier/). As the risk assess-ment provides information of possible species invasiveness,but not on whether the species actually becomes invasive inthe specific new habitat, finally, a simplified 3-level scale (1–3) was used to group aliens with varying invasive potentialand known invasiveness throughout Oahu. (Daehler et al.2004; Daehler and Baker 2006).
Leaf Terpene Extraction and Analysis Leaf samples werecrushed in liquid nitrogen with a Teflon pestle in a Teflontube until a homogeneous powder was obtained. Between2–4 ml of pentane (depending on the leaf type) were addedbefore the pulp defrosted. The Teflon tubes were main-tained airtight at 25°C during 24 h for full extraction. Afterthis, a sample of each extract was put into a 300 μl glassvial. Samples were injected automatically into the GC-MSfollowing a split of 0.5:80, thus allowing only 0.625% ofthe injected sample to enter the column. The column was anHP-5 crosslinked 5% PH Me Silicone (Supelco Inc.).Solvent delay was 3 min. The initial temperature of 40°Cwas increased immediately with a ramp of 30°C min−1 to60°C. The second ramp was 10°C min−1 to 150°C, whichwas maintained for 3 min. The third ramp was 70°C min−1
to 250°C, which was maintained for 5 min. Carrier gas washelium at 0.7 ml min−1. The mass detector was used with anelectron impact of 70 eV. Identification of monoterpeneswas conducted by GC-MS and comparison with authenticstandards from Fluka (Buchs, Switzerland), literature
spectra, and GCD Chemstation G1074A HP. Calibrationwith common terpenes α-pinene, 3-carene, β-pinene, β-myrcene, p-cymene, limonene, sabinene (monoterpene),and α-humulene (sesquiterpene) standards was carried outonce every 5 analyses. Standards were purchased fromSigma Aldrich (Gilingham, Dorset, UK). Terpene calibra-tion curves (N=4 different terpene concentrations) werealways highly significant (r2>0.99 for the relationshipsbetween signal and terpene concentrations). The mostabundant terpenes had similar sensitivity (differences wereless than 5%). Quantification of the peaks was conductedaccording to the amount of ion 93 in the compound and byusing the calibration of the most similar mono- orsesquiterpene standard depending on the compound inves-tigated. The total GC run time was 23 min. All samplingand analytical procedures were applied in the same way fornative and alien species.
Statistical Analyses The program Phylomatic (Webb andDonoghue 2005) was used to build a phylogenetic tree ofthe species studied (Fig. 1) as explained in Peñuelas et al.(2010). The stadistical significance of the genetic differ-ences among different species in explaining the variabilityof the studied variables was calculated by employingMatlab 7.6.0 with the PHYSIG module developed byBlomberg et al. (2003).
Altitude was significantly correlated with all the mainclimate variables of each respective site (total annualprecipitation, the precipitation of the three driest months,mean annual temperature, annual mean of the dailyminimum temperatures, annual mean of the daily maximumtemperatures, annual mean of monthly difference betweenthe maximum and minimum temperature and annual meanof the coldest monthly temperature) (data not shown).
To analyze the effects of all studied characteristics onfoliage terpene contents, we conducted a general linearmodel (GLM) with site (4 different sample sites), speciesorigin (native and alien), and soil type (5 different soiltypes) as independent categorical variables, altitude asindependent continuous variable, and in the case ofvariables with phylogenetic fingerprinting, phylogeneticdistances also were included as continuous independentfactors. We introduced the factor site in the GLM design toextract the variability due to site. Since the origin of thestudied species (native vs. alien) showed a significantphylogenetic signal (k=0.309, P=0.022) mainly due to thehigh abundance of alien species of the Orders Rosales,Lamiales, and Laurales, we conducted all the statisticalanalyses that had the origin of species as the independentfactor both by an ordinary GLM without phylogeneticdistance matrix and also with phylogenetic distance matrixeven when the dependent variable had no significantphylogenetic signal. Thereafter, the model with a lower
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Fig. 1 Phylogenetic tree of the studied woody plant species obtainedfrom PHYLOMATIC programme (Webb and Donoghue 2005). Thescale depicts millions of years. The field sampling site is depicted
between brackets to the right of each species. (SLH = St. LouisHeights. HV = Hahaione Valley. T = Tantalus. WR = WilliwillinuiRidge). The origin (N = Native. A = Alien) is also depicted
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Akaike information criterion (AIC) was selected. Toconduct these analyses we used Matlab 7.6.0 withREGRESSIONV2 module (Lavin et al. 2008). We alsoconducted a PCA analysis with leaf economics spectrumvariables (nutrients, Amass and LMA) and the different setsof species as cases. Then, we looked at the correlationbetween the factor scores that characterized the functionalspectrum and total leaf terpene contents by using Statistica6.0 software package (StatSoft, Inc. Tule, OK, USA).
We employed the same rationale to analyze potentialdifferences between native and alien species in terpenecontents vis-à-vis leaf chemical, physiological, and ana-tomical traits. To analyze what variables are differentlycorrelated between alien and native species, we conducteddiscriminant analysis among leaf total terpene contents andleaf traits by using Matlab 7.6.0 with REGRESSIONV2module (Lavin et al. 2008) and Statistica 6.0 software(StatSoft, Inc. Tule, OK, USA). To analyze the effects ofleaf economics spectrum on terpene emisssion and whetherthere were different relationships between native and alienspecies, we also conducted a PCA analysis with the speciesas cases and leaf economics spectrum (nutrients, amass, andLMA) as variables and calculated the factor scores for eachspecies. Thereafter, we conducted a correlation between thefactor scores that characterized the functional spectrum andthe total terpene contents.
To compare possible differences in the proportion of speciesthat produced and accumulated terpenes between the alien andnative species set, we conducted a Chi-square test by usingStatistica 6.0 software package (StatSoft, Inc. Tule, OK, USA).
Results
Foliage Terpene Concentration. Alien vs. Native SpeciesTwenty-five (10 natives and 15 alien) of the 73 studiedspecies contained at least one terpene (concentration abovethe detection limit of 0.6 ng g−1 in their leaves; Tables 2and 3). No terpenes were detected in 48 of the 73 studiedspecies (Appendix 1). Total terpene and total monoterpeneconcentrations were higher in the entire set of alien speciesthan in the entire set of native species (P=0.02 and P=0.04,respectively) (Table 4, Fig. 2). In alien species, total terpeneconcentration was 1965±367 μg g−1 (4524±1225 μg g−1
when considering only storing species) and in nativespecies it was 830±227 μg g−1 (2905±650 μg g−1 whenconsidering only storing species). Total sesquiterpenes,cyclic monoterpenes, cyclic sesquiterpenes, and aromaticmonoterpenes were also higher in alien than in nativespecies but the differences were not significant (Table 4,Fig. 2). The greater average total terpene content in alienthan in native species was due mainly to higher leaf
monoterpenes in moderately-high invasive species and tohigher sesquiterpenes in highly invasive species than innative species (Fig. 2). Neither the sampling site nor soiltype had any significant effect on total terpene content(Table 4). The proportion of species that accumulatedterpenes, although higher in alien species, was notsignificantly different between native (29%) and alienspecies (39%) (χ2=0.97, P=0.42).
Several mono- and sesquiterpene compounds werefound in 10 native species (Cheirodendron trigynum,Melicope clusiifolia, Melicope peduncularis, Metrosiderosmacropus, Metrosideros polymorpha, Metrosiderosrugosa, Metrosideros tremuloides, Myrsine lessertiana,Myrsine sandwicensis, Syzygium sandwicensis), whichhad not been described previously as terpene accumulatorsto our knowledge. Syzygium sandwicensis accumulated 3monoterpenes (camphene, E-β-ocimene, 3,7 dimethyl-octa-1,3,7-triene) and 11 sesquiterpenes (Tables 2 and 3)in its leaves. In the species of the genus Metrosideros,three monoterpenes (sabinene, 1,3,6-octatriene, 3,7-dimethyl E-β-ocimene) and 18 sesquiterpenes (Tables 2and 3) were detected. In the two species of the genusMyrsine, 2 monoterpenes (limonene, myrcene) and 33sesquiterpenes (Tables 2 and 3) were observed. InCheirodendron trigynum, 11 monoterpenes and 11 sesqui-terpenes were found (Tables 2 and 3). Finally, in the twoMelicope species, 24 monoterpenes and 29 sesquiterpeneswere found (Tables 2 and 3).
Among the 15 alien species that accumulated terpenes intheir leaves, three species Heliocarpus americanus (1monoterpene, 7 sesquiterpenes, Tables 2 and 3), Schinusterebinthifolius (7 monoterpenes, 9 sesquiterpenes), andPersea americana (7 monoterpenes, 3 sesquiterpenes) hadnot been reported previously as terpene accumulators.
Phylogenetic influence on the values of the variableswas present only in 6 of the 156 different detected terpenes:β-cubebene, β-maaliene, epi-bicyclo-sesqui-phellandrene,γ-elemene, β-ocimene and l-β-pinene. Total terpene con-tents did not show a phylogenetic effect (data not shown).
Relationships of Leaf Terpenes to Amass, LMA and NutrientLeaf Concentrations and Climate No significant relation-ships of total terpenes with climatic characteristics andAmass were observed in the corresponding GLM analysiseither in native or alien species (data not shown).Discriminant analysis of the total terpenes (TT) and leaftraits: LMA (Wilk’s Lambda = 0.58 and P=0.002), leaf Nconcentration (Wilk’s Lambda = 0.65 and P=0.008), leaf Kconcentration (Wilk’s Lambda = 0.82 and P=0.1) and Amass
(Wilk’s Lambda = 0.67 and P=0.019), separated native andalien species (Fig. 3), showing that the set of native specieshad greater LMA and lower leaf economic traits and leafterpenes than the set of alien species. Relationships of total
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terpene contents with the main leaf economic and structuraltraits did not differ between native and alien species(Fig. 3). There was no significant correlation between totalleaf terpenes and the PC1 scores of each species obtained inthe PCA analysis of leaf economic traits (LMA, Amass, N,K) within native plants (R=0.17, P=0.64) nor within alienplants (R=0.090, P=0.77) (Fig. 3).
Discussion
Terpenes in Hawaiian Plants This study provides novelinformation about terpene contents in Hawaiian native plantspecies. It also contributes to advance our understanding ofterpene content in several alien species that have worldwidedistributions (Sharma et al. 1999; Olajide et al. 1999;Ghisalberti 2000; Kikuzaki et al. 2000; Wheeler et al. 2002;Pino et al. 2005; Zhao et al. 2009).
None of the 10 native species that accumulated terpenes hasbeen reported previously as terpene-containing, at least to ourbest knowledge. At the genus level, only some species of thegenus Syzygium had been reported as terpene accumulators(Chang et al. 1999). Among the 15 alien terpene-containingspecies, six had been previously identified as mono andsesquiterpene-containing species (Psidium guajava, Olajide etal. 1999; Lantana camara, Sharma et al. 1999; Ghisalberti2000; Pimenta dioica, Kikuzaki et al. 2000; Melaleucaquinquenervia, Wheeler et al. 2002; Mangifera indica, Pinoet al. 2005; Ageratina adenophora, Zhao et al. 2009). In thesecases, the terpenes reported previously and those found in thepresent research generally were the same, but with somedifferences. Some terpenes found in Lantana camara, such asα-gurjunene or zingiberene, had not been reported previouslyin this species. Similarly, in Melaleuca quinquenervia, wefound 7 terpenes (viridiflorol, 1–8 cineole, α-terpineol, α-pinene, β-pinene, γ-terpinene, α-terpinene) of the 10 alreadypreviously reported in this species (Wheeler et al. 2002), butin addition we also found 8 more monoterpenes and 22sesquiterpenes (Tables 2–3). It is possible that the samplingtechnique may have induced some stress, which might haveresulted in the production of these extra compounds. Five ofthe 17 alien species that accumulated several mono- andsesquiterpenes, Cinnamomum burmannii, Eucalyptus robus-ta, Psidium cattleianum, Rubus rosifolius, and Syzygiumcumini (Tables 2–3) had not yet been reported as terpene-accumulator species, although members of the same genushave been described as terpene accumulators (Chang et al.1999; Olajide et al. 1999; Moore et al. 2004; Chao et al.2005; Yang et al. 2005; Malowicki et al. 2008). In anotherspecies, Pluchea carolinensis, known to have medicalproperties, terpene content has been suggested, but had notbeen described (Fernández and Torres 2006). In this study, 1
monoterpene and 3 sesquiterpenes were detected in thisspecies. Finally, three alien species Heliocarpus americanus,Schinus terebinthifolius and Persea americana had not beenreported previously as terpene accumulators. We did notdetect a phylogenetic effect in the total terpene content amongthe set of studied species, nor in the content of the individualterpenes.
Higher Terpene Content in Alien Species and No Relationshipto Leaf Economics In regard to the number of species thataccumulate terpenes, although the difference was not signif-icant, the proportion of species that accumulated terpenes inleaves was slightly higher in alien (39%) than in native (29%)species. In regard to the absolute terpene leaf accumulation,alien species accumulated greater amounts in leaves, and alsohad greater N and P leaf concentrations than native species,and their ratio of terpene contents to the concentrations ofthese two elements were higher than in native species. Thus,the differences between alien and native species wereproportionally greater in leaf terpene accumulation than in Nand P leaf content. Collectively, these data suggest a greaterinvestment in terpene production with respect to nutrientabsorption and carbon fixation in alien compared with nativespecies. Thus, alien species in Hawai’i may have moreproductive leaves and invest more of their leaf primaryproduction in terpene accumulation than native species.
The discriminant analyses based on the relationshipsbetween total terpene accumulation and LMA and nutrientcontent significantly separated alien from native plants, thusreflecting that alien species have greater total terpenecontents, N and K concentrations, and Amass and lowerLMA than native species. When comparing native withalien species, a significantly higher leaf nutrient and terpenecontent are observed in alien species. This segregationsuggests that these species may be using different resourcesand might also have greater capacities to capture and usenutrients. Despite this, however, there were no significantrelationships between leaf terpene accumulation and leafeconomic spectrum in either native or alien species.
“Nutrient Driving”,“Excess Carbon” and “EICA Related”Hypotheses The comparison of alien and native species didnot support the “excess carbon” hypotheses (Loomis 1932;Bryant et al. 1983; Herms and Mattson 1992; Peñuelas andEstiarte 1998). Alien species had higher N leaf contents butdid not have lower terpene concentrations. Decreases ofterpene production have been reported when leaf nutrientconcentrations increase (Son et al. 1998). Kainulainen et al.(1996) observed that N fertilization had no effect onmonoterpene concentrations in growing needles of Pinussylvestris, but in mature needles, N fertilization significant-ly decreased concentrations of some individual and totalmonoterpenes. There also are reports of no relationships at
216 J Chem Ecol (2010) 36:210–226
Spec
ies
Ori
gin
Age
rati
na a
deno
phor
aA
p-C
ymen
e34
0 ±
60
α-Pi
nene
27.3
±11
.2
Cam
phen
e70
7 +
105
β-Pi
nene
14 ±
12
Δ 3 -C
aren
e 18
.8 ±
5.9
Lim
onen
e91
± 1
2
Thy
moq
uino
ne33
1 ±
105
Bor
nyl a
ceta
te10
60 ±
172
α-T
erpi
nene
485
± 9
3E
ndo-
born
eol
30.6
± 3
.7
E-α
-O
cim
ene
20 ±
7
E-β
-O
cim
ene
11 ±
2
Lin
aloo
l21
± 6
Che
irod
endr
on tr
igyn
umN
α-T
huje
ne6.
3 ±
3.1
α-Ph
ella
ndre
ne13
0 ±
70
α-Pi
nene
3500
± 1
100
Sabi
nene
66 +
28
Cam
phen
e30
± 1
3β-
Pine
ne67
3 ±
533
β-T
erpi
nene
165
± 6
7α-
Ter
pino
lene
13 ±
5
α-C
amph
olen
eal
dehy
de36
± 2
0
α-T
erpi
nene
5 ±
2M
yrce
ne16
3 ±
66
Cin
nam
omum
bur
man
nii
Ap-
Cym
ene
220
± 1
00
Cam
phen
e67
± 2
1
β-Pi
nene
910
± 2
60
Δ 3 -
Car
ene
117.
0 +
3.0
Thy
moq
uino
ne45
± 9
E-α
-O
cim
ene
49.1
± 1
7
1,8-
Cin
eole
261
± 7
2
γ-T
erpi
nene
3.7
± 2
.6
α-T
erpi
nole
ne8
± 2
Ter
pine
n-4-
ol6
± 2
α-T
erpi
neol
79 ±
22
Ter
pino
lene
133
± 3
9
Myr
cene
72 ±
24
E-α
-Oci
men
e3.
6 ±
1.7
L-3
,7-d
imet
hyl-
1,3,
7-O
ctat
rien
e21
± 7
n. id
. mon
oter
pene
10 ±
5
Euc
alyp
tus
robu
sta
Ap- C
ymen
e77
± 1
1
α-Pi
nene
330
± 1
50α-
Fenc
hene
22 ±
5.6
7C
amph
ene
14 ±
11.
8Ph
ella
ndre
ne79
± 2
4L
imon
ene
33 ±
10
β-Ph
ella
ndr
ene
5.7
± 1
.4
α- Cam
phol
ene
alde
hyde
6 ±
1
E-
Pino
carv
eol
278
± 3
6
3-C
yclo
hexe
n-1-
ol. 4
-met
hyl-
1-(1
-m
ethy
leth
yl)-
7 ±
2
p-M
enth
a-1.
5.8-
trie
ne13
± 2
α- Ter
pine
ol41
± 1
7
Z-p
-Men
tha-
1(7)
,8-d
ien-
2-ol
6 ±
6
Bor
nyl f
orm
ate
15 ±
2E
ndo-
fenc
hol
35 ±
7E
ndo-
born
eol
74 ±
16
E-α
-Oci
men
e6
± 1
E-L
inal
ool O
xide
5.1
± 1
.6
Hel
ioca
rpus
am
eric
anus
AC
amph
ene
0.30
± 0
.22
Lan
tana
cam
ara
Aα-
Thu
jene
4.1
± 0
.4
α-Ph
ella
ndre
ne16
± 3
α-Pi
nene
105
± 1
0.7
Sabi
nene
90 ±
9C
amph
ene
43 ±
5.5
3Δ
3 -Car
ene
71.5
± 7
.8L
imon
ene
66 ±
14
l-C
amph
or61
± 9
α-T
erpi
neol
27 ±
4
α-T
erpi
nene
4.7
± 1
.9
Ter
pino
lene
14 ±
4
E-α
-O
cim
ene
18 ±
4
Lin
aloo
l31
± 7
Man
gife
ra in
dica
Aα-
Pine
ne10
.3 ±
0.7
f-Ph
ella
ndre
ne5
± 0
β-Ph
ella
ndre
ne30
± 1
E-α
-Oci
men
e1.
3 ±
0.5
E-β
-Oci
men
e3.
4 ±
1.3
Mel
aleu
ca q
uinq
uene
rvia
Aα-
Thu
jene
6.1
± 1
.5α-
Pine
ne74
6 ±
155
Cam
phen
e12
± 3
.85
β-Pi
nene
188
± 2
2
α -
Ter
pine
ne79
± 1
5
1,8-
Cin
eole
5963
± 6
05γ-
Ter
pine
ne85
± 1
7
α-T
erpi
nole
ne9
± 4
Isop
uleg
ol37
± 1
3-C
yclo
hexe
n-1-
ol. 4
-m
ethy
l-1-
(1-
met
hyle
thyl
)-15
± 2
α-T
erpi
neol
2155
± 4
13
- ex
o-2-
Hyd
roxy
cine
ole
17 ±
3
Myr
cene
32 ±
22
E-α
-Oci
men
e11
± 8
Lin
aloo
l82
± 2
5
Mel
icop
e cl
usii
foli
aN
p-C
ymen
e9
± 5
α-Pi
nene
3661
± 1
23C
amph
ene
15 ±
8.4
3β-
Pine
ne57
± 3
3L
imon
ene
31 ±
15
Z L
inal
ool o
xide
33 ±
19
α-C
amph
olen
eal
dehy
de98
± 5
7
E-P
inoc
arve
ol18
± 1
1E
-Ver
beno
l52
± 3
0M
yrte
nol
7 ±
3V
erbe
none
14 ±
8B
orny
l ace
tate
7 ±
3
End
o-bo
rneo
l6
± 1
Myr
cene
22 ±
4E
-β-O
cim
ene
4.8
± 0
.5L
inal
ool o
xide
56 ±
26
Lin
aloo
l18
± 8
Ger
anyl
ace
tate
27 ±
15
Mel
icop
e pe
dunc
ular
isN
α-Pi
nene
13 ±
6(1
R)-
E-I
solim
onen
e13
± 2
Lim
onen
e14
9 ±
113
β-T
erpi
nene
39 ±
17
p-M
enth
a-1.
5.8-
trie
ne6
± 3
E-C
arvy
l ace
tate
8 ±
6E
-α-O
cim
ene
1.6
± 0
.2p-
Men
tha-
E-2
,8-d
ien-
1-ol
9 ±
7
Tab
le2
Foliarcontentsof
arom
atic,cyclic,andno
n-cyclic
mon
oterpenes(μgg−
1)detected
inthestud
iednativ
eandalienspeciesin
Oahu(H
awai’i).The
specieslackingdetectable
amou
ntsof
arom
atic
andcyclic
mon
oterpenesareshow
nin
App
endix1.
A=alien;
N=nativ
e
J Chem Ecol (2010) 36:210–226 217
Met
rosi
dero
s m
acro
pus
NSa
bine
ne13
± 5
Met
rosi
dero
s po
lym
orph
aN
E-α
-Oci
men
e19
+ 5
E-β
-Oci
men
e56
± 1
7
Myr
sine
san
dwic
ensi
sN
Lim
onen
e1
± 1
Myr
cene
1.8
± 1
.0
Per
sea
amer
ican
aA
α-Ph
ella
ndre
ne6.
4 ±
0.2
α-Pi
nene
113
± 5
1Sa
bine
ne27
8 ±
27
β-Pi
nene
137
± 7
61,
8-C
ineo
le77
± 9
E S
abin
ene
hydr
ate
2.3
± 0
.2M
yrce
ne11
± 3
Pim
enta
dio
ica
Ap-
Cym
ene
0.13
± 0
.11
Eug
enol
4177
± 1
950
α-T
huje
ne9.
9 ±
8.1
α-Ph
ella
ndre
ne36
± 3
α-Pi
nene
26 ±
15
β-Pi
nene
1.2
± 1
.0Δ
3 -Car
ene
3.13
± 2
.61,
8-C
ineo
le13
3 ±
77
γ-T
erpi
nene
15 ±
12
α-T
erpi
nole
ne64
± 5
2
Ter
pine
n-4-
ol0.
17 ±
0.1
4α-
Ter
pine
ol6
± 5
Ter
pino
lene
30 ±
25
Myr
cene
9 ±
8
Plu
chea
car
olin
ensi
sA
α-Pi
nene
4 ±
68
Psi
dium
cat
tlei
anum
Aα-
Pine
ne26
± 2
1
Schi
nus
tere
bint
hifo
lius
Aα-
Thu
jene
75 ±
9α-
Phel
land
rene
730
± 7
3α-
Pine
ne11
15 ±
141
Sabi
nene
406
± 4
9β-
Thu
jene
2544
± 2
86α-
Ter
pine
ne84
± 2
1M
yrce
ne53
± 4
tE
-β-O
cim
ene
17 ±
2
Syzy
gium
cum
ini
Aα-
Phel
land
rene
2.6
± 0
.3
α-Pi
nene
110
± 2
0α-
Fenc
hene
1.6
± 0
.65
β-Pi
nene
65 ±
36
l-Ph
ella
ndre
ne27
± 3
Lim
onen
e16
7 ±
17
α-T
erpi
nole
ne5.
0 ±
1.9
α-T
erpi
neol
6 ±
2α-
Ter
pine
ne10
7 ±
10
Ter
pino
lene
0.2
± 0
.1M
yrce
ne 17
+ 2
E-α
-Oci
men
e1.
5 ±
0.5
Syzy
gium
san
dwic
ensi
sN
Cam
phen
e12
± 1
E-β
-Oci
men
e52
3 ±
120
L-3
,7-d
imet
hyl-
1,3,
7-O
ctat
rien
e68
± 6
218 J Chem Ecol (2010) 36:210–226
Spec
ies
Ori
gin
Age
rati
na a
deno
phor
aA
Sab
inyl
acet
ate
67.9
+7.
0
E-α
-B
erga
mot
ene
10+
1
β-C
aryo
phyl
lene
501
+91
β-Fu
nebr
ene
130
+21
α-B
erga
mot
ene
410
+60
α-L
ongi
pine
ne14
.3+
6.4
Ger
mac
rene
-D44
8+
366
α-Z
ingi
bere
ne78
.4+
14.2
Bic
yclo
-ge
rmac
rene
330
+56
β-B
isab
olen
e61
2+
118
β-Se
squi
phel
land
rene
284
+57
Cis
-α-B
isab
olen
e17
6+
49
Cad
ina-
1,4-
dien
e15
+6
γ-C
urcu
men
e17
93+
232
α-B
isab
olol
1484
+21
6
E-
Car
yoph
ylle
ne17
+3
E-β
-Far
nese
ne47
3+
105
σ-N
erol
idol
71+
9N
erol
idol
124
+36
1(5)
,6-G
uaia
dien
e23
85+
341
Cal
aren
e11
9+
22
Che
irod
endr
on tr
igyn
umN
α-C
opae
ne10
+2
β-C
aryo
phyl
lene
7+
2
α-H
umul
ene
187
+14
6G
erm
acre
ne-D
491
+22
0α-
Zin
gibe
rene
230
+16
8E
rem
ophi
lene
116
+54
β-Se
squi
phel
land
rene
39+
21
Ger
mac
rene
B84
+24
Cyc
lois
olon
gifo
l-5-
OL
(ses
qui)
4.6
+0.
6
Deh
ydro
-ar
omad
endr
ene
7+
2
(3E
,5E
,8Z
)-3,
7,11
-T
rim
ethy
l-1,
3,5,
8,10
-dod
ecap
enta
nene
3.8
+1.
2
Cin
nam
omum
bur
man
nii
Aβ-
Car
yoph
ylle
ne43
1+
112
Ger
mac
rene
-D52
6+
123
Bic
yclo
-ge
rmac
rene
-62
6+
114
E−α
-B
isab
olen
e63
+16
γ−E
lem
ene
36+
11Sp
athu
leno
l14
3+
68C
aryo
phyl
lene
oxid
e36
7+
17G
uaio
l15
2+
49Is
ospa
thul
enol
8+
2α-
Eud
esm
ol18
+6
Euc
alyp
tus
robu
sta
AA
lloar
oma-
dend
rene
13+
5G
lobu
lol
1.6
+0.
3
Hel
ioca
rpus
am
eric
anus
Aα-
Cub
eben
e6
+1
β-E
lem
ene
3.2
+2.
0C
is-α
-Bis
abol
ene
0.6
+0.
5β-
Sel
inen
e36
+7
α-Se
linen
e31
+6
Car
yoph
ylle
neox
ide
25+
3γ-
Gur
june
ne21
+4
Lan
tana
cam
ara
Aα-
Cop
aene
11+
3
β-C
aryo
phyl
lene
773
+10
6
α-H
umul
ene
645
+79
Ger
mac
rene
-D64
4+
107
α-Z
ingi
bere
ne43
+5
β-C
ubeb
ene
43+
7B
icyc
lo-g
erm
acre
ne68
0+
105
Ger
mac
rene
A86
+17
α-G
urju
nene
115
+17
E−α
-Bis
abol
ene
5+
2
Man
gife
ra in
dica
Aβ-
Car
yoph
ylle
ne24
+1
α-H
umul
ene
12.9
+0.
3β-
Cub
eben
7+
0.3
α-G
urju
nene
18+
1G
erm
acre
neB
140
+21
γ-C
urcu
men
e26
+14
Mel
aleu
ca q
uinq
uene
rvia
Aα-
Cop
aene
49+
6α-
Gur
june
ne57
+4
β-C
aryo
phyl
lene
276
+9
Allo
arom
aden
dren
e43
+19
Aro
mad
endr
ene
224
+24
α-H
umul
ene
56+
0.3
Ger
mac
rene
-D2.
1+
0.9
β-Se
linen
e13
8+
35
Deh
ydro
arom
aden
dren
e38
+0.
5
α-Se
line
ne15
2+
25
α-A
mor
phen
e13
9+
22
Δ-C
adin
ene
120
+15
Glo
bulo
l70
+12
Ver
idif
loro
l38
11+
714
Led
ol63
4+
141
α-C
opae
ne89
+12
γ-E
udes
mol
99+
22α-
Eud
esm
ol33
6+
68β-
Eud
esm
ol10
1+
64α-
Am
orph
ene
43+
3P
alus
trol
92+
14C
aryo
phyl
lene
oxid
e19
7+
35
Mel
icop
e cl
usii
foli
aN
Z-C
aryo
phyl
lene
52+
1A
rom
aden
dren
e49
2+
230
α-H
umul
ene
1442
+50
Ari
stol
ene
26+
13β-
Sel
inen
e89
+20
γ-C
adin
ene
221
+11
3Δ-
Cad
inen
e37
6+
199
Epi
glob
ulol
47+
27β-
Car
yoph
ylle
ne13
16+
77Sp
athu
len
ol48
+1
Car
yoph
ylle
neox
ide
792
+23
4Is
oled
ene
28+
9
β-E
udes
mol
52+
19G
lobu
lol
188
+58
Cal
aren
e18
+1
α-E
udes
mol
145
+21
Mel
icop
e pe
dunc
ular
isN
α-C
opae
ne16
+7
β-G
uaie
ne9
+6
α-H
umul
ene
142
+25
Ere
mop
hile
ne10
+3
β-C
aryo
phyl
lene
10+
4G
erm
acre
neB
28+
8Sp
athu
leno
l52
+27
Car
yoph
ylle
neox
ide
70+
43
Gua
iol
1082
+20
9
E-
Car
yoph
ylle
ne6
+5
γ-E
udes
mol
173
+37
Cal
aren
e13
5+
25
Met
rosi
dero
s m
acro
pus
Nα-
Hum
ulen
e42
+14
E-C
aryo
phyl
lene
450
+16
7α-
Eud
esm
ol31
9+
31β-
Eud
esm
ol25
2+
60B
ulne
sol
186
+78
Met
rosi
dero
s po
lym
orph
aN
α-C
opae
ne63
+51
β-C
aryo
phyl
lene
1022
+33
β-E
lem
ene
26+
5
α- Hum
ulen
e14
5+
53
2-Is
opro
pyl-
5-B
icyc
lo[4
.4.0
]Dec
-1-e
n26
+11
γ-Se
linen
e41
+7
Ger
mac
rene
-D25
+20
β-S
elin
ene
665
+15
6α-
Selin
ene
783
+18
1
α-G
urju
nene
8+
4
γ-C
adin
ene
10.2
+5.
7
Δ-C
adin
ene
128
+70
α-M
uuro
lene
2.3
+1.
9
Car
yoph
ylle
neox
ide
9+
3
Epi
-B
icyc
lose
squi
phel
land
rene
13+
9
γ-G
urju
nene
27+
15Ju
nipe
ne3.
3+
1.7
Met
rosi
dero
s ru
gosa
Nα-
Cub
eben
e10
7+
50α-
Yla
ngen
e33
+14
α-C
opae
ne32
4+
144
β-C
aryo
phyl
lene
349
+14
0
β-C
ubeb
ene
379
+15
9A
rom
aden
dren
e24
+10
α-H
umul
ene
115
+46
2-Is
opro
pyl-
5-B
icyc
lo[4
.4.0
]Dec
-1-e
n13
9+
58
Ger
mac
rene
-D68
1+
317
α-A
mor
phen
e12
7+
61
α-G
urju
nene
76+
33
Ere
mop
hile
ne14
2+
90γ-
Cad
inen
e36
9+
159
α-M
uuro
lene
50+
22G
erm
acre
neB
433
+22
4L
edol
-27
+12
Δ-S
elin
ene
108
+10
T-M
uuro
lol 61
+49
(3S,
4R,5
S,6R
,7S)
-Ari
stol
-9-e
n-3-
ol8
+3
α-C
adin
ol 166
+71
Cad
ina-
1,4-
dien
e13
5+
65
γ-G
urju
nene
6+
4Δ-
Cad
inen
e66
3+
303
Tab
le3
Foliarcyclicsesquiterpenecontents(μgg−
1)in
nativ
eandalienspeciesin
Oahu(H
awai’i).Species
with
outdetectablesesquiterpenepo
olsarelistedin
App
endix1.
A=alien;
N=nativ
e
J Chem Ecol (2010) 36:210–226 219
Met
rosi
dero
s tr
emul
oide
sN
α-H
umul
ene
4.9
+2.
4G
erm
acre
ne-D
192
+11
9B
icyc
lo-g
erm
acre
ne9
+16
E-C
aryo
phyl
lene
15+
7
Myr
sine
less
erti
ana
Nα-
Cop
aene
48+
16
(3Z
)-C
embr
ene
A35
+12
β-C
aryo
phyl
lene
1091
+59
3
α- Ber
gam
oten
e8
+2
Allo
arom
aden
dren
e1.
1+
0.1
Aro
mad
endr
ene
12+
3α-
Hum
ulen
e29
4+
15
2-Is
opro
pyl-
5-B
icyc
lo[4
.4.0
]Dec
-1-e
n8
+2
γ- Selin
ene 19
9+
46
Ari
stol
ene
20+
6β-
Selin
ene
686
+21
4
β-C
ubeb
ene
244
+16
9
α-Se
linen
e82
5+
266
γ-M
uuro
lene
84+
22Δ-
Cad
inen
e16
3+
47Sp
athu
leno
l83
+38
Car
yoph
ylle
neox
ide
87+
33
T-
Muu
rolo
l15
+5
γ-C
adin
ene
40+
9
Myr
sine
san
dwic
ensi
sN
α-C
ubeb
ene
77+
19
α-Y
lang
ene
34+
11α-
Cop
aene
298
+54
β-C
aryo
phyl
len
e66
9+
160
Allo
arom
aden
dren
e11
+5
α-H
umul
ene
108
+20
Ger
mac
rene
-D57
0+
147
β-C
ubeb
ene
41+
10
Bic
yclo
-ge
rmac
rene
379
+16
6
α-A
mor
phen
e38
8+
159
α-G
urju
nene
9+
3Δ-
Cad
inen
e54
7+
158
α-M
uuro
lene
3.6
+2.
1Sp
athu
len
ol11
+3
Car
yoph
ylle
neox
ide
19+
2Is
oled
ene
11+
2α-
Cad
inol
87+
20C
alar
ene
51+
8C
adin
a-1,
4-di
ene
30+
4γ-
Gur
june
ne2.
9+
0.4
T-M
uuro
lol
98+
52Ju
nipe
ne21
0+
114
Per
sea
amer
ican
aA
Ger
mac
rene
-D
122
+27
β-C
ubeb
ene
58+
9Δ-
Cad
inen
e27
+12
Pim
enta
dio
ica
Aα-
Yla
ngen
e1.
6+
0.6
β-C
aryo
phyl
lene
399
+16
3β-
Ele
men
e4.
9+
3.9
Aro
mad
endr
ene
24+
19α-
Hum
ulen
e93
+39
Δ-C
adin
ene
47+
19C
aryo
phyl
lene
oxid
e31
+13
Cal
aren
e9
+4
γ-G
urju
nene
3.6
+1.
5T
-Muu
rolo
l4.
2+
2.5
Plu
chea
car
olin
ensi
sA
γ-G
urju
nene
77+
55α-
Selin
ene
41+
30α-
Gur
june
ne19
+9
Psi
dium
cat
tlei
anum
Aα-
Cub
eben
e30
+10
α-Y
lang
ene
43+
3α-
Cop
aene
385
+37
β-M
aalie
ne23
+3
β-C
aryo
phyl
lene
3132
+33
1A
lloa
rom
aden
dren
e39
+32
Aro
mad
endr
ene
55.8
+7.
5α-
Hum
ulen
e65
1+
47E
pizo
nare
153
+15
Ger
mac
rene
-D57
+8
β-S
elin
ene
122
+15
α-S
elin
ene
160
+23
α-A
mor
phen
e10
6+
8
γ-C
adin
ene
165
+33
Δ-C
adin
ene
355
+29
E-γ
-Bis
abol
ene
79+
7
α-M
uuro
lene
57+
5
Ger
mac
rene
B35
3+
99
Car
yoph
ylle
neox
ide
73+
7
Ver
idif
loro
l37
+6
Val
ence
ne19
7+
39
6,10
,11,
11-T
etra
met
hyl-
tric
yclo
[5-3
-0-1
(2,3
)und
ec-
1(7)
ene
48+
4
E-β
-Fa
rnes
ene
27+
8
Cal
aren
e21
+3
γ- Cur
cum
ene
116
+36
γ- Gur
june
ne41
+7
α-B
isab
olol
43+
18
Juni
per
cam
phor
67+
6
Psi
dium
gua
java
Aα-
Yla
ngen
e18
+7
α-C
opae
ne21
+17
β-M
aalie
ne37
+12
β-C
aryo
phyl
lene
454
+12
9
Allo
arom
aden
dren
e4.
7+
3.0
Aro
mad
endr
ene
132
+50
α-H
umul
ene
48+
15G
erm
acre
ne-D
12+
4β-
Selin
ene
46+
27α-
Selin
ene
110
+51
α-A
mor
phen
e33
0+
104
γ-C
adin
ene
124
+55
Δ-C
adin
ene
242
+12
1
E-γ
-B
isab
olen
e21
1+
85
α-M
uuro
lene
36+
11C
aryo
phyl
lene
oxid
e34
+5
Ver
idif
loro
l0.
5+
0.4
Val
ence
ne0.
6+
0.5
6,10
,11,
11-T
etra
met
hyl-
tric
yclo
[5-3
-0-1
(2,3
)und
ec-1
(7)e
ne28
+10
Cal
aren
e16
+5
γ-C
urcu
men
e20
+3
α-B
isab
olol
135
+49
E-β
-Far
nese
ne36
+16
Ger
mac
rene
B12
+6
Rub
us r
osif
oliu
sA
α-C
ubeb
ene
50+
23α-
Yla
ngen
e69
+31
α-C
opae
ne16
4+
74G
erm
acre
ne-D
29+
13β-
Cub
eben
e78
+34
α-A
mor
phen
e83
9+
381
γ-C
adin
ene
28+
13Δ-
Cad
inen
e19
4+
86β-
Cop
aen-
4α-
ol90
.4+
39.3
6,10
,11,
11-T
etra
met
hyl-
tric
yclo
[5-3
-0-
1(2,
3)un
dec-
1(7)
ene
499
+21
8
15-
Cop
aeno
l46
+21
T-M
uuro
lol
255
+10
9ca
ryop
hyll
a-3,
8(13
)-di
en-5
β-ol
9+
5
Schi
nus
tere
bint
hifo
lius
Aα-
Cop
aene
32+
3β-
Car
yoph
ylle
ne23
1+
77β-
Ele
men
e92
+15
α-H
umul
ene
38+
9G
erm
acre
ne-D
4710
+82
3B
icyc
lo-g
erm
acre
ne20
95+
521
Δ-E
lem
ene
202
+43
Ger
mac
rene
B30
2+
72E
-Car
yoph
ylle
ne30
+13
6,10
,11,
11-T
etra
met
hyl-
Syzy
gium
cum
ini
Aα-
Cop
aene
6+
2
β-E
lem
ene
89+
28α-
Gua
iene
56+
9α-
Hum
ulen
e19
6+
23G
erm
acre
ne-D
226
+23
Ari
stol
ene
46+
3G
erm
acre
neA
5700
+53
3γ-
Cad
inen
e41
.9+
3.0
Δ-E
lem
ene
56+
12α-
Muu
role
ne41
+7
Ger
mac
rene
B67
+6
Val
ence
ne0.
2+
0.2
tric
yclo
[5-3
-0-
1(2,
3)un
dec-
1(7)
ene
139
+16
Isol
eden
e27
2+
53
Cal
aren
e32
+4
Glo
bulo
l42
+18
E-C
aryo
phyl
lene
423
+53
Syzy
gium
san
dwic
ensi
sN
α-C
ubeb
ene
14+
1α-
Cop
aene
0.30
+0.
01A
rom
aden
dren
e26
.5+
0.2
α-H
umul
ene
21+
0.4
β-C
ubeb
ene
21+
0.3
α-G
urju
nene
16+
0.3
Δ-G
uaie
ne2.
8+
0.4
Led
ol15
+0.
3Is
oled
ene
23+
1C
adin
a-1,
4-di
ene
12+
2E
-Car
yoph
ylle
ne31
+1
220 J Chem Ecol (2010) 36:210–226
Tab
le4
Meanvalues
(SE)of
theconcentrations
ofthemostabun
dant
terpenes
andtheirratio
sto
keynu
trient
contentsandph
otosyn
thetic
capacity
perdrymass(A
mass)in
relatio
nto
sampling
site,speciesorigin
(nativeor
alien)
andsoiltype.P-valuesindicate
theresults
ofgenerallin
earmod
els.OLS-O
rdinaryleastsquaresregression
(see
“Metho
ds”)
Trait
Mod
elSite
1Origin
Soil2
Ta
Wi
HV
SLH
P-value
Native
Alien
P-value
Inc
Oxi
Ult
Inc_T
Moll
P-value
β-Caryo
phyllene
μg
g−1
OLS
45.5
84.6
351
61.4
0.60
89.7
164
0.72
022
147
.869
.049
.90.94
(30.6)
(51.3)
(201
)(42.0)
(46.0)
(86)
(0)
(48)
(32.1)
(69.0)
(49.9)
α-H
umuleneμg
g−1
OLS
0.85
102
95.5
135
0.82
71.4
45.8
0.67
39.6
110
0.65
15.2
11.7
0.86
(0.65)
(58)
(54.8)
(9)
(41.9)
(24.1)
(32.0)
(48)
(0.65)
(13.6)
(11.7)
Caryo
phyllene
oxideμg
g−1
OLS
1.7
38.7
8.8
20.7
0.46
27.9
10.5
0.96
021
.71.8
49.2
390.58
(1.7)
(31.7)
(5.0)
(17.8)
(22.7)
(5.6)
(0)
(22.7)
(1.8)
(49.2)
(39)
Myrcene
μg
g−1
OLS
3.94
8.1
3.3
3.8
0.51
5.3
5.1
0.49
2.8
6.9
4.1
8.1
1.2
0.78
(3.42)
(6.5)
(3.3)
(2.0)
(4.7)
(2.4)
(2.8)
(4.9)
(3.6)
(8.1)
(1.2)
p-Cym
eneμg
g−1
OLS
26.6
0.36
07.0
0.53
0.3
16.7
0.06
30
0.26
28.0
19.2
0.02
0.78
(18.7)
(0.36)
(0)
(7.0)
(0.3)
(10.6)
(0)
(0.26)
(19.7)
(19.2)
(0.02)
α-Phelland
rene
μg
g−1
OLS
43.6
5.3
46.6
3.3
0.94
3.7
44.8
0.18
0.4
25.0
45.8
04.5
0.97
(43.6)
(5.2)
(45.5)
(3.3)
(3.7)
(30.2)
(0.4)
(21.9)
(45.8)
(0)
(4.5)
α-Pineneμg
g−1
OLS
12.8
291
83.1
101
0.41
164
74.0
0.97
18.3
242
13.4
270
3.2
0.54
(7.6)
(198
)(69.2)
(71)
(142
)(35.4)
(18.3)
(144
)(7.9)
(177
)(3.2)
Cam
pheneμg
g−1
OLS
33.7
2.3
2.7
2.4
0.72
1.6
20.4
0.18
02.9
35.4
6.5
00.96
(33.7)
(1.4)
(2.7)
(1.6)
(1.0)
(18.6)
(0)
(1.5)
(35.4)
(3.8)
(0)
β-Pineneμg
g−1
OLS
7.2
31.8
017
.20.36
20.8
10.7
0.80
10.8
20.8
7.1
46.9
0.15
0.63
(6.5)
(26.9)
(0)
(17.1)
(11.2)
(6.2)
(10.8)
(19.2)
(6.8)
(46.9)
(0.15)
Total
mon
oterpene
μg
g−1
OLS
247
291
360
1360
0.14
195
693
0.04
487
.135
826
926
1455
80.24
(161
)(197
)(313
)(904
)(101
)(304
)(84.1)
(197
)(169
)(228
7)(558
)
Total
sesquiterpeneμg
g−1
OLS
545
1150
1433
676
0.75
635
1272
0.08
1321
1250
560
1748
84.8
0.56
(454
)(391
)(628
)(313
)(202
)(297
)(122
6)(346
)(478
)(166
4)(84.8)
Total
terpeneμg
g−1
OLS
792
1141
1793
2034
0.42
830
1965
0.03
914
0816
0781
943
70(642
0.12
(660
)(465
)(875
)(148
8)(227
)(367
)(131
0)(470
)(640
)(394
2)(642
)
Total
mon
oterpene/N
μgTerpmg−
1N
OLS
1018
.717
.4118
0.04
712
.847
.40.01
4.5
20.6
10.3
243
410.02
9
(5.8)
(13)
(15.4)
(83)
(9.3)
(13.3)
(43)
(11.5)
(6.0)
(216
)(41)
Total
mon
oterpene/P
μgTerp
mg−
1P
OLS
180
328
223
3275
0.04
222
21153
0.22
93.1
321
188
6527
1239
0.00
34
(120
)(219
)(201
)(234
7)(158
)(700
)(87.6)
(179
)(107
)(160
)(123
9)
Total
sesquiterpene/N
μgTerpmg−
1N
OLS
19.3
81.6
80.6
62.3
0.46
52.8
67.7
0.40
71.2
82.9
19.4
163.5
622
0.14
(14.6)
(28.0)
(34.0)
(57.3)
(19.5)
(23.8)
(61.7)
(23.1)
(15.3)
(156
.9)
(6.2)
Total
sesquiterpene/PμgTerpmg−
1P
OLS
293
1637
1449
1759
0.14
961
1346
0.36
1469
1443
298
4509
188
0.22
(199
)(545
)(505
)(161
3)(361
)(540
)(126
3)(404
)(210
)(444
0)(188
)
J Chem Ecol (2010) 36:210–226 221
all between soil nutrients and terpene contents (Heyworth etal. 1998). Our results support the “nutrient driving synthesishypothesis”, which expects higher nutrient availability totranslate into higher carbon fixation and activity of theenzymes involved in isoprenoid production (Harley et al.1994; Litvak et al. 1996). Other studies have reported asignificant and positive relationship between leaf terpenecontent and N availability in Pinus halepensis (Kainulainenet al. 2000), and NPK fertilization has shown to increaseterpene contents in Chrysanthemum boreale (Lee et al.2005). On the other hand, our results also support themodified EICA related hypothesis that suggests that aliensuccess may be favored by an increase in the concentrationsof less costly defenses such as terpenes that may be moretoxic to generalist herbivores (Joshi and Vrieling 2005;Stastny et al. 2005), as has been observed in some previousstudies (Johnson et al. 2007).
Terpene Content and Success of Aliens The results suggestthat alien success may be related to higher levels of leafterpene content that can have protective effects in responseto environmental stress and/or prevent the attack ofgeneralist herbivores and pathogens. The possible role ofterpenes as cause of alien success due to herbivorismprotection, however, should be taken with caution becausethe few studies that have examined herbivory pressure inHawai’i are inconclusive. For example, a study by DeWaltet al. (2004) found little fungal and insect damage on oneinvader; however, Joe and Daehler (2008) found significantslug damage on several rare native species. Terpenes mayproduce advantages by other mechanisms, e.g., overallhigher terpene production and accumulation in alien speciescould be involved in allelopathic or protective mechanismsT
Fig. 2 Foliar benzenic monoterpene (BMT), cyclic monoterpene(CMT), cyclic sesquiterpene (CST), non-cyclic monoterpene (NCMT),non-cyclic-sesquiterpene (NCST), total monoterpene (TMT), totalsesquiterpene (TST), and total terpene (TT) concentrations (μg g−1) innative and alien species grouped according to their invasiveness index.Different letters indicate statistically significant differences at P<0.05among species groups with differing invasiveness index
222 J Chem Ecol (2010) 36:210–226
that would confer competitive advantage with respect tonative species, compensating for their greater nutritivevalue and palatability that results from their higher nutrientcontents and lower LMA. Additionally, terpenes have otherfunctions that can confer competitive advantage to aliens.For example, they have infochemical and communicationroles (Peñuelas et al. 1995; Wheeler et al. 2002; Peñuelasand Llusià 2003, 2004), and confer photoprotection(Peñuelas and Munné-Bosch 2005) and thermotolerance(Sharkey and Singsaas 1995; Peñuelas and Llusià 2001 and2002; Peñuelas et al. 2005). They also may confer
protection against drought stress (Kainulainen et al. 1991;Llusià and Peñuelas 1998), and may act as generalantioxidants, protecting vital membranes against peroxida-tion and reactive oxygen species such as singlet oxygen(Loreto and Velikova 2001; Peñuelas and Llusià 2002;Loreto et al. 2004; Munné-Bosch et al. 2004; Llusià etal. 2005).
In summary, total terpene contents were greater in alienthan in native species. The frequency of leaf terpene-containing species, however, was not significantly greaterin alien than in native species. The results also suggest that
Ag
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Fig. 3 Discriminant analysisusing Leaf total terpenes (TT) vs.Photosynthetic capacity (Amass),TT vs. Leaf mass per area(LMA), TT vs. leaf nitrogenconcentration (N), TT vs. Leafpotassium concentration, TT andTT vs. PC1 first principal com-ponent factor scores of ‘leafeconomics spectrum’ (covaria-tion among leaf traits; LMA,A-mass, N, K ) as independentcontinuous variables, and speciesorigin: native (in black - bold)and alien (in red – light gray) asthe dependent categorical factor.Only terpene containing speciesare considered in the discrimi-nant analyses shown here. Simi-lar results were found for thewhole set of species studiedincluding both terpene containingand non-containing species.(Ag = Ageratina adenophara,Cb = Cinnamonium burmanii,Ct = Cheirodendrum trigynum,Er = Eucapyptus robusta, He =Heliocarpus americanus, Lc =Lantana camara, Ma = Metrosi-deros macropus, Mc = Melicopeclusiifolia, Md = Myrsine les-sertiana, Me = Metrosiderospolimorpha, Mi = Magniferaindica, Mp = Melicope peduncu-laris, Mq = Melicope quinque-nervia, Mr = Metrosiderosrugosa, Ms = Myrsine sandwi-censis, Mt = Metrosideros trem-uloides, Pc = Plucheacarolinensis, Pd = Pimentadioica, Pe = Persea Americana,Pg = Psidium guajava, Pt =Psidium cattleionum, Ru =Rubus rosifolius, Sc = Syzygiumcumini, St = Schinnus terebinthi-folius, Sy = Syzygiumsandwisensis)
J Chem Ecol (2010) 36:210–226 223
the percentage of species that contain terpenes in leaves inOahu is probably comparable with other floras. Alien speciespresented higher terpene contents, and also greater N and Kleaf concentrations, and Amass, but lower LMA than nativespecies. These differences between alien and native speciesdid not support the “exces carbon” and the “traditionalEICA” hypothesis but were in accordance with the “nutrientdriven synthesis” and with the “modified EICA related”hypotheses. The results suggest a possible different time-stage of adaptation to a novel Oahu habitat between native(old-alien-invaders) and recent alien plants. The differentpatterns in production and content of terpenes in native andalien species merit further investigation, given that plantinvasive success is an emerging global phenomenon.
Acknowledgements ÜN was holding G. P. Wilder Chair at theDepartment of Botany, University of Hawai’i at Manoa, Hawai’iduring the time of the study. We also thank the students, faculty, andstaff of that Department for making available laboratory space andequipment for this research. This research was supported by grantsfrom the Spanish Government (CGL2006-04025/BOS andConsolider-Ingenio Montes CSD 2008-00040), the Catalan Govern-ment (SGR 2009-458), Estonian Science Foundation (grant 7645), andthe Estonian Ministry of Education and Science (SF1090065s07).
Appendix 1. Species with not detected foliar terpenecontents in this study
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