Higher Allocation to Low Cost Chemical Defensesin Invasive Species of Hawaii

Josep Peñuelas & J. Sardans & J. Llusia & S. M. Owen &

J. Silva & Ü. Niinemets

Received: 30 June 2010 /Revised: 8 September 2010 /Accepted: 15 September 2010 /Published online: 25 September 2010# Springer Science+Business Media, LLC 2010

Abstract The capacity to produce carbon-based secondarycompounds (CBSC), such as phenolics (including tannins)and terpenes as defensive compounds against herbivores oragainst neighboring competing plants can be involved inthe competition between alien and native plant species.Since the Hawaiian Islands are especially vulnerable toinvasions by alien species, we compared total phenolic(TP), total tannin (Tta), and total terpene (TT) leaf contentsof alien and native plants on Oahu Island (Hawaii). Weanalyzed 35 native and 38 alien woody plant speciesrandomly chosen among representative current Hawaiianflora. None of these CBSC exhibited phylogenetic finger-printing. Alien species had similar leaf TP and leaf Ttacontents, and 135% higher leaf TT contents compared withnative species. Alien plants had 80% higher leaf TT:N leafcontent ratio than native plants. The results suggest thatapart from greater growth rate and greater nutrient use,alien success in Oahu also may be linked to greater contentsof low cost chemical defenses, such as terpenes, asexpected in faster-growing species in resource rich regions.The higher TT contents in aliens may counterbalance their

lower investment in leaf structural defenses and their higherleaf nutritional quality. The higher TT provides highereffectiveness in deterring the generalist herbivores of theintroduced range, where specialist herbivores are absent. Inaddition, higher TT contents may favor aliens conferringhigher protection against abiotic and biotic stressors. Thehigher terpene accumulation was independent of the alienspecies origin, which indicates that being alien eitherselects for higher terpene contents post-invasion, or thatspecies with high terpene contents are pre-adapted toinvasiveness. Although less likely, an originally lowerterpene accumulation in Hawaiian than in continental plantsthat avoids the increased attraction of specialist enemiesassociated to terpenes may not be discarded.

Key Words Alien species . Chemical defenses . Physicaldefenses . Hawaii . Invasive species . LMA . Nitrogen .

Phosphorus . Phenolics . Phylogeny . Tannins . Terpenes

Introduction

Plant invasive success is one of the most important aspectsof current global biosphere change (Mooney and Hobbs,2000). It severely threatens biodiversity (Lodge, 1993) andcan result in great economic cost (Normile, 2004). Tropicalvolcanic island ecosystems appear to be especially vulner-able to invasive species. Some studies suggest that currentnative species developed on the original poor soils of theislands, and have poor ability to capture resources (Allisonand Vitiusek, 2004). The increasing resources availabilityover time make island communities especially vulnerable tothe establishment and spread of alien species, especially ongeologically old islands with well-weathered rich soils(Allison and Vitiusek, 2004). The Hawaiian Islands, the

J. Peñuelas (*) : J. Sardans : J. Llusia : S. M. Owen : J. SilvaGlobal Ecology Unit CREAF-CEAB-CSIC, CREAF, Edifici C,Universitat Autònoma de Barcelona,08913 Bellaterra, Catalonia, Spaine-mail: josep.penuelas@uab.cat

S. M. OwenCentre for Ecology and Hydrology Edinburgh (CEH),Penicuik EH26 0QB Scotland, Great Britain

Ü. NiinemetsInstitute of Agricultural and Environmental Sciences,Estonian University of Life Sciences,Kreutzwaldi 1,Tartu 51014, Estonia

J Chem Ecol (2010) 36:1255–1270DOI 10.1007/s10886-010-9862-7

most isolated ecosystem of the Earth (Vitousek and Walker,1989), are particularly vulnerable to invasions by non-indigenous species (Harrington and Ewel, 1997). Hawaiiannative ecosystems and plant species are strongly affected byalien plant species (Mack and D’Antonio, 2003; Hughesand Denslow, 2005; Hughes and Uowolo, 2006). In theHawaiian Islands, around 861 flowering plant species (47%of total Hawaiian angiosperm flora) are naturalized alienspecies (Wagner et al., 1999), that have been introducedmainly in the last 200 years (Smith, 1996).

The capacity to produce carbon based secondary com-pounds (CBSC) such as phenolics, tannins, and terpenes,can be involved in the competition between alien and nativeplant species by conferring chemical defenses againstherbivores, allelochemical defenses against neighboringcompeting plants (Peñuelas et al., 1996; Peñuelas andEstiarte, 1998; Kursar and Coley, 2003; Mote et al., 2007;Cipollini et al., 2008; Khanh et al., 2008), or/and greateranti stress capacity (Peñuelas and Llusià, 2003, 2004;Filella and Peñuelas, 1999).

Phenolics, including low molecular mass phenolics andcondensed polyphenolics such as tannins act by reducingdigestibility rather than through direct toxicity (Eichhorn etal., 2007), but many of them also have toxic effects, and maybe more toxic for some herbivores than for others (Mole etal., 1990; Cipollini et al., 2008). They are effective mainlyagainst specialist herbivores (Beck and Schoonhoven, 1980;Coley et al., 1985; Bernays and Chapman, 1994; Bennet andWallsgrove, 1994). Nevertheless, several studies also havedemonstrated that they can inhibit the growth of generalistherbivores (Eck et al., 2001; Kouki and Manetas, 2002;Nomura and Itioka, 2002; Albrectsen et al., 2004; Boege andDirzo, 2004; Kurokawa and Nakashizuka, 2008), althoughnot always (Bi et al., 1997; Goverde et al., 1999; Mutikainenet al., 2000). Terpenes act as deterrents, toxins or modifiersof insect development (Bennet and Wallsgrove, 1994). Theyare effective against non adapted specialist herbivores(Sorensen et al., 2005), and generalist herbivores (Mihaliaket al., 1987; Landau et al., 1994; Mote et al., 2007).Moreover, terpenoids have many other protective propertiessuch as defense against fungi and pathogens (Gershenzonand Duradeva, 2007), and against abiotic stresses such ashigh temperature, drought, ozone, or excess radiation(Peñuelas and Llusià, 2003, 2004).

Many hypotheses and theories have been proposed in thelast few decades to explain plant defensive strategy againstherbivores. They range from theories based on plantcapacity to allocate resources in excess of growth demandsinto defenses, such as a “carbon excess” hypothesis (Bryantet al., 1983; Peñuelas and Estiarte, 1998), to theories withmore evolutionary bases (Hamilton et al., 2001) that bypasstheories on enhanced terpenoid production as a result ofenhanced nutrient availability (Harley et al., 1994; Litvak et

al., 1996; Peñuelas and Staudt, 2010). Some of thesetheories, mainly those based on “carbon excess”, have beenhighly criticized and mostly dismissed (Hamilton et al.,2001; Koricheva, 2002; Nitao et al., 2002). Alien successcould bring new clues to this topic. In fact, the role of plantdefense allocation in invasive success has been widelydiscussed, and some theories such as “Evolution ofIncreased Competitive Ability” (EICA) hypothesis (Blosseyand Nötzold, 1995) were proposed to link plant defensestrategy with alien success. For example, a recent approachof EICA proposes that selection may favor a reduction inthe expression of metabolically expensive chemicaldefenses effective against specialist herbivores (Müller-Schärer et al., 2004; Lankau, 2007) but instead favor anincrease of the contents of less costly qualitative defenseseffective against general herbivores such as terpenes (Joshiand Vrieling, 2005; Stastny et al., 2005).

We aimed to study the link between the plant invasivesuccess in the Oahu (Hawaii) flora and CBSC contents.With this purpose, we conducted an analysis of leaf totalphenolic (TP), leaf total tannin (Tta), and leaf total terpene(TT) accumulation in 35 native and 38 alien woody plantspecies randomly chosen among the most representativecurrent Hawaiian flora in order (i) to compare TT, Tta, andTP contents of native plants with those of alien plants aftertaking into account the phylogenetic effects, and (ii) tocompare also the relationships of TT, Tta, and TP contentswith the leaf traits linked to foliar economy and productioncapacity, such as photosynthetic capacity (Amass), leafmass per unit area (LMA), and leaf N, P, and K contents.With these investigations, we additionally aimed to test thepredictions of some of the CBSC hypotheses such as the“excess carbon” hypotheses (decreased phenolics andtannins in alien nutrient-rich fast-growing species),nutrient-enhanced terpene production, and the modified“competitive ability” hypotheses (increased less costlyterpene accumulation against generalist herbivores anddecreased more costly phenolic and tannins accumulationagainst adapted herbivore specialists in alien species).

Methods and Materials

Field Sites

The study was conducted in May 2007 on the island ofOahu (Peñuelas et al., 2010; Sardans et al., 2010), the thirdlargest of the Hawaiian Islands. As typical of largerHawaiian Islands, the climate is characterized by steeprainfall gradients over short distances (Müller-Dombois andFosberg, 1998). While precipitation is distributed almostuniformly in lowland and mountain rain forests, lowlands atthe leeward side have a pronounced dry summer season.

1256 J Chem Ecol (2010) 36:1255–1270

Due to the oceanic tropical climate, temperature oscillationsare small with winters having on average 2–3°C coolertemperatures than summers. As large differences in com-position of native and alien vegetation occur in response torainfall gradients, four sites with distinct precipitationregimes were selected for plant sampling in the leewardlowlands of Oahu and at the leeward side of Koolaumountains (Appendix Table 1) (see details in Peñuelas etal., 2010).

The four key soil types found across the sites rankaccording to the state of weathering as oxisols > ultisols >mollisols > inceptisols (Uehara and Ikawa, 2000; Deenikand McClellan, 2007). More leached oxisols and ultisolswith lower pH are among the soils with lowest fertility, andMollisols exhibit the highest fertility (Uehara and Ikawa,2000; Deenik and McClellan, 2007). Inceptisols, theyoungest soils, typically show weak profile development,and exhibit tremendous variability in fertility depending ongenesis (Deenik and McClellan, 2007). While the incepti-sols in rocky soils and mountainous land are of low fertility,the Tantalus series inceptisols are of moderate to highfertility. Thus, in our study, the broad soil classes rankaccording to fertility as mollisols > inceptisols (Tantalus) >oxisols ≅ ultisols > inceptisols (mountainous soils).

Plant Sampling and Site Climate

For each species, 3 individual plants were sampled. Severaltwigs per plant were sampled in the morning hours between8:00–12:00. Species coordinates and sampling altitude werenoted for each site, and this information was used to linkspecies locations to specific soil types and derive location-specific climatic data. We used ARCGIS 9.1 to determinelong-term average monthly and annual precipitation, andprecipitation of the 3 driest months and annual precipita-tion, and average, maximum and minimum temperaturesfrom high resolution climatic grids (Giambelluca et al.,1986, T. Giambelluca unpublished data) (see details inPeñuelas et al., 2010).

Study Species

Altogether 73 species, randomly sampled in the 4 sites, werestudied, 35 native and 38 aliens (Peñuelas et al., 2010). Outof the 73 studied species, 36 were trees, 29 shrubs, 3 woodyvines to shrubs, 3 woody vines, one subshrub, and onemistletoe (Sardans et al., 2010) (Appendix Table 2). Once anindividual of a given abundant species was randomlyselected, then we were looking non-randomly for 2 moreindividuals of the given species. The event of speciesselection, however, was random. Also, in drier sites,dominated by a few species, we sampled essentially allwoody species.

Species were classified according to site preference asdry, dry-mesic, mesic, dry-wet, mesic-wet, and wet forestspecies. The invasiveness of species was quantitativelyscored by using a four-level scale as 0 (native species), 1(low invasiveness), 2 (moderate-high), and 3 (very high).These scores were based on Australia/New Zealand weedrisk assessment (WRA) system scores (Pheloung et al.,1999) modified to Hawaii and other Pacific Islands(Daehler et al., 2004) that are reported in Pacific IslandEcosystems at Risk (PIER) project online database main-tained by U.S. Forest Service’s Institute of Pacific IslandsForestry (http://www.hear.org/pier/), and on recent updateson species invasive potential in Oahu (Daehler and Baker,2006). For species not quantitatively scored in theseassessments, species invasiveness was based on authors’observations on species abundance, presence of seedlings,and capacity of vegetative reproduction throughout theleeward ecosystems in Oahu. Although the overall riskscore assessment provides 32 scales for the scored species,we used a simplified scoring with 4 ranks to make it morerobust.

Chemical Analyses

Total phenolic content (TP) of leaves was determined bythe improved Folin-Ciocalteu assay (Singleton and Rossi,1965; Marigo, 1973). The improvement relative to standardassay was the use of a blank of polyvinylpolypyrrolidone(PVPP). PVPP retains the phenolic compounds avoidingtheir reaction with Folin-Ciocalteu solution, thereby pro-viding a true blank sample. For extraction of phenols,15 mg of dried pulverized leaf sample with 10 ml methanol:water (70:30 v/v) extraction solution were incubated for30 min in an ultrasound bath at 40°C. Thereafter, themixture was centrifuged for 10 min at 10000 rpm. Two (Aand B) aliquots of 1 ml were obtained from each sampleand added to a 25 ml volumetric flask. One aliquot (B) wasbrought to pH 3.5 with 0.1 M HCl and mixed with 0.5 g ofPVPP during 10 min. Sixteen ml of distilled water thenwere added to both samples A and B, and 1 ml of Folin-Ciocalteau reagent to each one of the flasks. After 3 min ofincubation at 40°C, 2 ml of a saturated NaCO3 (20%)solution was added to each one of the samples, and distilledwater were added until 25 ml. The samples were incubatedat 40°C for an additional 20 min, and the absorbances ofthe samples, A and B were determined at 760 nm usinga spectrophotometer Helios Alpha (Thermo Spectronic,Cambridge, UK).

Total soluble tannins (Tta) were extracted from 20 mg ofleaf powder with 12 ml of 70% acetone. Tubes containingthe sample and the acetone were sonicated three times for1 min allowing the tubes to cool for 3 min betweensuccessive sonications. After centrifugation, the extract was

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assayed with the butanol/HCl method (Porter et al., 1986)modified as in (Makkar and Goodchild, 1996). Briefly,0.5 ml of the extract was mixed with 3 ml butanol-HCl(95:5) and 0.1 ml of ferric reagent (ferric ammonium sulfatein 2 N HCl) and kept in a boiling water bath for 60 min.After cooling the tube, absorbance was measured at 550 nmby spectrophotometer Helios Alpha. Non-heated replicatetubes for each extract were used as anthocyanins blank, andits absorbance was substracted from the absorbance of theheated tubes. The Tta content on a dry weight basis wasestimated by using a 1 cm wide cuvette (Porter et al., 1986;Makkar and Goodchild, 1996). Tta analyses were con-ducted in triplicate.

For terpene analysis, the leaves of each species werecrushed in liquid nitrogen with a Teflon pestle in a Teflontube until a homogeneous powder was obtained. Afterhomogenization, 1 ml of pentane was added before the pulpdefrosted. The tubs were maintained at 25°C during 24 h,and after this period a sample of each extract was put into a300 μl glass vial. Samples were injected automatically intoa GC-MS (HP 6800 series 2, Hewlett Packard, Palo Alto,CA, USA) following a split of 0.5:50. Solvent delaywas 3 min. The initial temperature of 40°C was immedi-ately increased with a ramp of 30°Cmin-1 to 60°C. Thesecond ramp rate was 10°Cmin-1 to 150°C, which was heldfor 3 min. The third ramp rate was 70°Cmin-1 to 250°C,which was held for 5 min. The carrier gas was helium at0.7 mlmin-1. A mass selective detector was used with anelectronic impact of 70 ev. The identification of mono-terpenes was conducted by GC-MS comparing with stand-ards from Fluka (Buchs, Switzerland), literature spectra,and GCD Chemstation G1074A HP and Willey 7n spectralibrary. Frequent calibrations (once every 5 analyses) withα-pinene, 3-carene, β-pinene, β-myrcene, p-cymene, lim-onene, sabinene, and α-humulene standards were used forquantification. Terpene calibration curves (N=4 differentterpene contents) were always highly significant (r2>0.99for the relationships between signal and the amount ofterpene standard injected). The most abundant terpenes hadsimilar sensitivity (differences were less than 5%). Thequantification of the terpene peaks were conducted usingthe ion with mass 93 in the fractionation spectrum. Thetotal GC run time was 23 min. All processes wereperformed in the same way for native and alien species.

Statistical and Phylogenetic Analyses

The program Phylomatic (Webb and Donoghue, 2005) wasused to build a phylogenetic tree of the species studied(Fig. 1). Briefly, this program assembles a phylogeny forthe species of interest employing a backbone plant mega-tree based on a variety of sources involving primarily DNAstudies. Our phylogenetic hypothesis was based on the

conservative megatree, where unresolved nodes wereincluded as soft politomies. We employed programs in thePDAP package (Garland et al., 1993) to transform thephylogenetic tree into a matrix of phylogenetic distances,and assessed whether the studied traits showed significantphylogenetic signal—i.e., the tendency of closely relatedspecies to resemble each other due to shared ancestry—employing the randomization procedure in the PHYSIGmodule developed by Blomberg et al. (2003). This testconsists in comparing the variance in phylogenetic inde-pendent contrasts observed in the real dataset against a nulldistribution obtained after the phenotypic data wererandomized across the tips of the phylogeny (i.e., breakingany pattern of phylogenetic resemblance between relatives).Phylogenetic signal was considered significant if thevariance in contrasts of the real dataset was lower thanthe variance in 95% of the permuted datasets. To performcomparisons across traits, we employed the k statistic thatestimates how much phylogenetic signal is present in thephenotypic data compared against the expectation from arandom walk model of phenotypic evolution (Blomberg etal., 2003). If k=1, then the phenotypic trait has exactly theamount of signal expected for the phylogenetic treeemployed and a model of evolution of random walk(Brownian motion); k>1 indicates a stronger phylogeneticresemblance than expected; and k<1 the opposite pattern.These analyses were performed to determine if phyloge-netic correction was necessary in subsequent regressionanalyses. We employed generalized linear models (GLM) toanalyze how total leaf phenolics, tannins, and terpenesvaried as a function of species origin (native or alien) thatwas included as independent categorical variable.

The sampling altitude (relative to sea level) correlatedsignificantly with the main climate variables of eachrespective site (total annual precipitation, the precipitationof the three driest months, mean annual temperature, annualmean of the daily minimum temperature, annual mean of thedaily maximum temperature, annual mean of the monthlytemperature fluctuation, and annual mean of the coldesttemperature of each month) (data not shown). Because ofthis, altitude was used as covariate in all the conductedgeneral linear models in order to take into account the effectsthat climate could have on the analyzed leaf variables.

To analyze the sources of variation in total phenolic,total tannin, and total terpene contents, we conducted ageneral linear model (GLM) with site (4 different samplesites), species origin (native and alien), and soil type (5different soil types) as independent categorical variables,altitude as independent continuous variable, and in the caseof variables with phylogenetic fingerprinting, phylogeneticdistances also included as continuous independent factor.To conduct these analyses we used Matlab 7.6.0 withREGRESSIONV2 module (Lavin et al., 2008).

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We employed the same rationale to analyze potentialdifferences between native and alien species in the ratios oftotal phenolics, tannins, and terpene contents relative to leafchemical, physiological and anatomical traits: foliar N andP contents, foliar photosynthetic capacity (Amass), andLMA reported in a previous study of these species(Peñuelas et al., 2010). We also conducted discriminantanalyses with pairwise combinations of leaf total phenolicswith leaf N and P contents, Amass, and LMA as continuousindependent variables and species origin (alien or native) asa grouping variable. As described above, ordinary leastsquares (OLS) GLM or Phylogenetic general least square(PGLS) GLM analyses were selected depending on the

significance of the phylogenetic fingerprinting (see above).We conducted a principal component analysis (PCA) withleaf economics spectrum (LMA, Amass, [N], and [P]) asvariables, and then correlated the factor scores (PC1 andPC2) with the leaf contents of phenolics, tannins, andterpenes. We also conducted a PCA with the leaf contentsof phenolics, tannins, and terpenes to investigate whethernative and alien species were significantly separared bythese variables. Thereafter, we used the PC1 and PC2scores of this PCA to correlate with LMA, Amass, [N], and[P]. To test whether the observed frequency of alien speciesthat accumulated terpenes was equal in the differentcontinents of origin we conducted a Chi-square analysis.

Williwillinui ridge (WR)

Tantalus Hahaione valley (HV)

St. Louis Heights (SLH)

Acacia confusaAcacia koaSenna surattensisDesmodium incanumFalcataria moluccanaHaematoxylum campechianumCasuarina equisetifoliaFicus macrophyllaFicus microcarpaTrema orientalisRubus rosifoliusAntidesma platyphyllumBischofia javanicaOchna thomasianaPassiflora suberosaElaeocarpus bifidusEucalyptus robustaMelaleuca quinquenerviaMetrosideros macropusMetrosideros polymorphaMetrosideros rugosaMetrosideros tremuloidesSyzygium cuminiSyzygium sandwicensisPimenta dioicaPsidium cattleianumPsidium guajavaHeliocarpus americanusHibiscus arnottianusSida fallaxWiskstroemia oahuensisMangifera indicaSchinus terebinthifoliusMelicope clusiifoliaMelicope peduncularisAgeratina adenophoraPluchea carolinensisScaevola gaudichaudianaClermontia oblongifoliaCheirodendron trigynumIlex anomalaIlex paraguariensisAlyxia stellataLabordia tinifoliaBobea elatiorCoffea arabicaCoprosma longifoliaHedyotis acumiataHedyotis fosbergiiHedyotis terminalisBuddleja asiaticaCitharexylum caudatumClerodendrum macrostegiumLantana camaraStachytarpheta cayennensisJasminum fluminenseTabebuia roseaCestrum nocturnumCarmona retusaArdisia ellipticaMyrsine lessertianaMyrsine sandwicensisDiospyros sandwicensisPouteria sandwicensisVaccinium calycinumBroussaisia argutaKorthalsella complanataSantalum freycinetianumPisonia umbelliferaCinnamomum burmanniiPersea americanaFreycinetia arboreaSmilax melastomifolia

0100200300

Native

Alien

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L

Acacia confusaAcacia koaSenna surattensisDesmodium incanumFalcataria moluccanaHaematoxylum campechianumCasuarina equisetifoliaFicus macrophyllaFicus microcarpaTrema orientalisRubus rosifoliusAntidesma platyphyllumBischofia javanicaOchna thomasianaPassiflora suberosaElaeocarpus bifidusEucalyptus robustaMelaleuca quinquenerviaMetrosideros macropusMetrosideros polymorphaMetrosideros rugosaMetrosideros tremuloidesSyzygium cuminiSyzygium sandwicensisPimenta dioicaPsidium cattleianumPsidium guajavaHeliocarpus americanusHibiscus arnottianusSida fallaxWiskstroemia oahuensisMangifera indicaSchinus terebinthifoliusMelicope clusiifoliaMelicope peduncularisAgeratina adenophoraPluchea carolinensisScaevola gaudichaudianaClermontia oblongifoliaCheirodendron trigynumIlex anomalaIlex paraguariensisAlyxia stellataLabordia tinifoliaBobea elatiorCoffea arabicaCoprosma longifoliaHedyotis acumiataHedyotis fosbergiiHedyotis terminalisBuddleja asiaticaCitharexylum caudatumClerodendrum macrostegiumLantana camaraStachytarpheta cayennensisJasminum fluminenseTabebuia roseaCestrum nocturnumCarmona retusaArdisia ellipticaMyrsine lessertianaMyrsine sandwicensisDiospyros sandwicensisPouteria sandwicensisVaccinium calycinumBroussaisia argutaKorthalsella complanataSantalum freycinetianumPisonia umbelliferaCinnamomum burmanniiPersea americanaFreycinetia arboreaSmilax melastomifolia

Fig. 1 Phylogenetic tree of theHawaiian plant species studied.The phylogenetic tree wasconstructed with the programPHYLOMATIC (Webb andDonoghue, 2005). The figurealso shows a map of the foursampling areas

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An ANOVA test also was conducted to test for differentterpene content depending on the continent of origin. Weused Matlab 7.6.0 with REGRESSIONV2 module (Lavin etal., 2008) and Statistica 6.0 software (StatSoft, Inc. Tulsa,OK, USA).

Results

Total Leaf Phenolic, Tannin, and Terpene Contents

Appendix Table 3 shows the species values of totalphenolics (TP), total tannins (Tta), and total terpenes(TT). They ranged between 8 and 159 mgg-1 DW, 1 and36 mgg-1 DW, and 0 and 13 mgg-1 DW, respectively(Appendix Table 3). All analyzed species exhibited detect-able contents of TP and Tta, whereas only 25 out of the 73species analyzed had detectable contents of terpenes(Appendix Table 3). Neither TP nor Tta nor TT contentspresented significant phylogenetic fingerprinting. Neithersoil type nor sampling site had significant effects on leaftotal phenolics (TP) (P=0.12 and P=0.62, respectively),total tannins (Tta) (P=0.45 and P=0.74, respectively), ortotal terpenes (TT) (P=0.31 and P=0.70, respectively).

Terpenes were detected in 13 alien species and in 12native species. The frequencies observed were not differentfrom the frequencies expected under the hypothesis ofequal frequency of leaf terpene accumulation in thedifferent continents of origin (observed X2=2.12 that waswithin the range of X2=7.81 that includes the 95% of thedistribution at d.f=3). Overall, alien species had higher(135%; P=0.039) leaf TT contents compared with nativespecies, but did not have significantly different total leafphenolic and tannin contents (Fig. 2). The different levelsof species invasiveness had no significant effect on TP andTta contents either, but TT contents increased withincreasing species invasiveness, considering only terpene-containing species (Fig. 2). There were no differences inleaf terpene content among invasive species of differentcontinent origins (one-way ANOVA, P=0.67). The PCAfor all the CBSCs did not separate alien from native species(data not shown). Only terpene contents were differentbetween alien and native species (Fig. 2). The CBSC PCAscores did not correlate either with the PCA scores forphysiological foliar economic spectrum traits (data notshown).

Relationships with Foliar Nutrient Contents,Amass, and LMA

Appendix Table 3 shows the species values of the TP:N,TP:P, Tta:N, Tta:P, TT:N, and TT:P ratios. The ranges ofthese ratios among the studied species set were broad,

showing great differences among species. The ranges ofTP:N and TP:P ratios were 0.4–18.2 gg-1 and 2.9–394 gg-1,respectively. The ranges of Tta:N and Tta:P ratios were0.05–3.11 gg-1 and 0.8–74.5 gg1, respectively. The rangesof TT:N and TT:P ratios were 0–15 gg-1 and 0–428 gg-1,respectively (Appendix Table 3). None of those ratiosexhibited significant phylogenetic fingerprinting.

Despite having higher foliar N content (Peñuelas et al.,2010), aliens had higher leaf TT:N content ratio (80%; P=0.03) compared with native plants (Fig. 3), reflecting muchhigher terpene content. No significant effects of samplingsite or soil type were observed on the ratios between leafTT content and leaf economic traits (data not shown).

The ratio between phenolic contents and photosyntheticcapacity was 50% lower in alien species compared with nativespecies (P=0.011). There was no other effect of speciesorigin, sampling site, or soil type on the ratios of leaf TP andTta contents relative to the leaf economic traits (Fig. 4).

In native species, TP was negatively correlated with leafN, and leaf P contents and Amass. In alien species, TP was

10

20

30

40

50

60

70

80

a abb

Native

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0

10

20

30

40

50

60

70

80

Total Poly-phenolics

Total Tannins Total Terpenes(in overall species)

Total Terpenes(in containing

species)

bbb

a

aab

abab

NativeLow invasivenessModerate-high invasivenessHigh invasiveness

Co

mp

ou

nd

co

nte

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(mg

g-1

)

Fig. 2 Total leaf phenolics (mgg-1), total leaf tannins (mgg-1) andtotal leaf terpenes (mgg-1) in native and alien species, and dependingon the invasiveness index. Significant differences (P<0.05) betweennative and alien species are indicated by different letters.Total terpenesare shown calculated for the overall set of species studied and alsoonly for the species containing terpenes

1260 J Chem Ecol (2010) 36:1255–1270

significantly correlated only with leaf P content (Fig. 5). Incontrast, we did not observe any significant relationships ofTta and TT contents with nutrient contents or with Amass

(data not shown).The discriminant analyses of TP and leaf [N] (Wilk’s

Lambda=0.85, P=0.003), TP and leaf [P] (Wilk’s Lambda=0.84, P=0.008), and TP and Amax (Wilk’s Lambda=0.84,P=0.006) separated alien from native species due to theirhigher N and P contents and Amass.

Discussion

Alien species had similar total leaf phenolic (TP) and tannin(Tta) contents but higher leaf total terpene (TT) contents thannative plants, with no phylogenetic signal in the differences.Moreover, alien species had higher leaf N and P contents,and Amass than native species, and, as a result, alien specieshad a lower leaf phenolics content/photosynthesis ratio thannative species, thus suggesting a lower relative effort onaccumulating leaf phenolics. Conversely, the total terpenecontent relative to N and P contents was larger in alien thanin native species. These greater contents of terpenes,providing more qualitative (more dependent on their toxicitythan on their quantity) lower cost chemical defenses againstgeneralist herbivores, may counterbalance the lower leafstructural defenses and higher leaf nutritional quality of alienplants. Alien plants thus would be able to deter herbivoreattacks using a different strategy of defense. On the other

hand, the higher terpene accumulation was independent ofthe continent of origin of the alien species (Asia, Australia,the Americas, Africa), which indicates that being alien eitherselects for higher terpene contents post-invasion, or thatspecies with high terpene contents are pre-adapted toinvasiveness.

Another possibility to explain these results is that theHawaiian environment is unusual in some sense thatselected for lower terpene levels in the past, and so thereal pattern is not that invasive plants have higher terpenesthan natives, but Hawaiian plants have lower terpenes thatcontinental species. In that case, the higher terpene levels ofthe alien species may not have any functional role ininvasion, but simply be a result of Hawaiian plants havinglow concentration of terpenes. With our current knowledge,however, this possibility does not seem likely. Terpenecontents have proven not to be determined phylogenetical-ly, at least in this study, suggesting that this capacity iswidespread throughout the entire plant taxa spectrum.Certainly, terpenes have been proven to accumulate inresponse to some climatic stresses (Peñuelas and Llusià,2003, 2004) but in this regard, the climate conditions of thenatural habitats of alien species are similar in most cases toHawaiian climate. Moreover, the percentage of species thataccumulate terpenes was not different between native andaliens showing that the capacity to produce and accumulateterpenes is not different although alien species accumulategreater amounts of terpenes. The number of studies thathave conducted a terpene screening in an extensive number

0

4

8

To

tal l

eaf

ph

eno

lics/

N

(g g

-1)

50

100

To

tal l

eaf

ph

eno

lics/

P

(g g

-1 )

0

0.4T

ota

l lea

f ta

nn

ins/

N

(g g

-1)

0

10

20

To

tal l

eaf

tan

nin

s/P

(g g

-1)

0

0.1

Native Alien

To

tal l

eaf

terp

enes

/N

(g g

-1)

a

b

0

2

Native Alien

To

tal l

eaf

terp

ene/

P

(g g

-1)

Fig. 3 Ratios of Total leafphenolics, total leaf tannins andtotal leaf terpenes relative toleaf N and P contents (gg-1).Significant differences (P<0.05)between native and alien speciesare indicated by different letters

J Chem Ecol (2010) 36:1255–1270 1261

of species in different regions of the world is, however,scarce, and to clearly discern whether or not terpeneaccumulation capacity is differently distributed throughoutthe world is not possible at this moment.

Some recent studies of the changes in chemical defensesin alien populations relative to non-alien populations of thesame species have reported that invasive populationsevolve a greater resistance to generalist herbivores (e.g.,Legar and Forister, 2005). In temperate grassland systems,higher concentrations of toxic secondary compounds alsohave been found in invaders. The explanation seems to bethat these compounds are not only defensive againstgeneralists but also attractive to specialists. Thus, in thenative range, the plants are constrained from evolvinghigher levels due to increased attraction of specialistenemies. In the introduced range where specialist herbi-vores are absent, the plants can invest more resources todefenses such as terpenes against generalist herbivores(Joshi and Vrieling, 2005). Previous studies also haveobserved no loss of defenses against generalist herbivoresin alien species populations (Leger and Forister 2005;

Hull-Sanders et al., 2007). The allocation to lower costdefenses such as terpenes should be more compatible with alow LMA and high photosynthetic capacity (Lankau,2007). This strategy can be especially successful for alienplants in environmentally rich sites, such as wet tropicalenvironments where higher growth and production providesa greater ability to compete for space occupation andresources uptake. Higher terpene contents are compatiblewith a fast return strategy of “leaf economics spectrum”

Lo

g10

To

tal p

hen

olic

s(m

g g

-1)

AcAk

Se

Di

FmHc

Ce

Fa

Fi

To

Ru

Ap

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

Sy

Pd

PtPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

CoCt

Ia

Ip

As

Lt

Be

Ca

Cl

Ha

Hf

Ht

Bs

Ci

Cm

Lc

Sh

JfTr

Cn

CrAe

Md

MsDsPs

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

0,8 1,0 1,2 1,4 1,6

Log10 N (mg g-1)

Log10 P (mg g-1)

0,8

1,2

1,6

2,0

2,4

R = 0.40, P = 0.018, Log10 TP = 2.6 - 0.84 Log10 N

AcAk

Se

Di

FmHc

Ce

Fa

Fi

To

Ru

Ap

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

Sy

Pd

PtPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

CoCt

Ia

Ip

As

Lt

Be

Ca

Cl

Ha

Hf

Ht

Bs

Ci

Cm

Lc

Sh

JfTr

Cn

CrAe

Md

Ms DsPs

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

-0,4 -0,2 0,0 0,2 0,4 0,6

0,8

1,2

1,6

2,0

2,4

R = 0.50, P = 0.002, Log10 TP = 1.51 - 0.73 Log10 PR = 0.33, P = 0.045, Log10 TP = 1.6 - 0.50 Log10 P

AlienNative

Ak

Di

Hc

Ce

Fa

Fi

To

Ru

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

SyPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

Ct

Ia

Ip

As

Lt

BeCl

Ha

Hf

Ht

Bs

Cm

Lc

Sh

JfTr

Cn

Cr

Md

Ms

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

-2 -1,6 -1,2 -0,8 -0,4 0

Log10 (Amass)

0,8

1,2

1,6

2,0

2,4

R = 0.31, P = 0.086, Log10 TP = 1.05 - 0.44 Log10 Amass

AcAk

Se

Di

FmHc

Ce

Fa

Fi

To

Ru

Ap

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

Sy

Pd

PtPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

CoCt

Ia

Ip

As

Lt

Be

Ca

Cl

Ha

Hf

Ht

Bs

Ci

Cm

Lc

Sh

JfTr

Cn

CrAe

Md

MsDsPs

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

0,8 1,0 1,2 1,4 1,6

0,8

1,2

1,6

2,0

2,4

R = 0.40, P = 0.018, Log10 TP = 2.6 - 0.84 Log10 N

AcAk

Se

Di

FmHc

Ce

Fa

Fi

To

Ru

Ap

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

Sy

Pd

PtPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

CoCt

Ia

Ip

As

Lt

Be

Ca

Cl

Ha

Hf

Ht

Bs

Ci

Cm

Lc

Sh

JfTr

Cn

CrAe

Md

Ms DsPs

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

-0,4 -0,2 0,0 0,2 0,4 0,6

0,8

1,2

1,6

2,0

2,4

R = 0.50, P = 0.002, Log10 TP = 1.51 - 0.73 Log10 PR = 0.33, P = 0.045, Log10 TP = 1.6 - 0.50 Log10 P

AlienNative

Ak

Di

Hc

Ce

Fa

Fi

To

Ru

Bj

OtPb

Eb

Er

Mq

Ma

MeMr

Mt

Sc

SyPg

He

Hi

Si

Wo

MiSt

McMp

Ag

Pc

Sg

Ct

Ia

Ip

As

Lt

BeCl

Ha

Hf

Ht

Bs

Cm

Lc

Sh

JfTr

Cn

Cr

Md

Ms

Vc

Ba

Kc

Sf

Pi

Cb

Pe

Fr

Sm

-2 -1,6 -1,2 -0,8 -0,4 0

0,8

1,2

1,6

2,0

2,4

R = 0.31, P = 0.086, Log10 TP = 1.05 - 0.44 Log10 Amass

Fig. 5 Relationships between total log10 leaf phenolics (mgg-1) andlog10 leaf N (mgg-1), log10 leaf P (mgg-1) contents, and log10 Amass

(μmols g-1s-1)

0

800

1600

To

tal l

eaf

ph

eno

lics/

Am

ass (a)

(b)

0

80

To

tal l

eaf

tan

nin

s/A

mas

s

0

30

60

Native Alien

To

tal l

eaf

ter

pen

es/A

mas

s

Fig. 4 Total leaf phenolics (mgg-1)/Amass (μmols g-1s-1), total tannins(mgg-1)/Amass (μmols g-1s-1) and total leaf terpenes (mgg-1)/Amass

(μmols g-1s-1) ratios. Significant differences (P<0.1) between nativeand alien species are indicated by different letters between brackets

1262 J Chem Ecol (2010) 36:1255–1270

based on a higher photosynthetic capacity, higher nutrientcontent, lower LMA, and faster return on investment infoliage (Wright et al., 2004). These traits help to explain thesuccess of invasive plant species (Pattison et al., 1998;Baruch and Goldstein, 1999; Funk and Vitousek, 2007)since they can contribute to faster growth rates for invadersand confer a competitive advantage over native species(Reich et al., 1997; Blumenthal and Hufbauer, 2007).Peñuelas et al., (2010) have observed these faster returnsfrom their investments in nutrients and dry mass in leaves,and these higher contents of most nutrients in these alienspecies in Oahu (Hawaii).

The higher terpene contents and higher nutrient contentsfit better the hypotheses based on higher nutrient availabil-ity translating into higher carbon fixation and activity of theenzymes involved in terpene production (Harley et al.,1994; Litvak et al., 1996; Peñuelas and Staudt, 2010) thanthe hypotheses based on carbon nutrient balance (Bryant etal., 1983; Peñuelas and Estiarte, 1998). The data for nativespecies fits the latter hypotheses but the data for alienspecies does not. Total phenolic contents were inverselycorrelated with foliar N and P contents and Amass in thenative species, but this did not happen in alien species,except for foliar P content. Phenolics are especially activedefenses against specialist herbivores (Coley et al., 1985;Bennet and Wallgrove 1994). Thus, in native plants, thepresence of specialist herbivores placed species along acontinuous gradient between a high allocation to defense(high phenolics content) and low leaf production capacity(low leaf nutrient content) to a low allocation to defense(low phenolics content) and high allocation to leafproduction capacity (high nutrient content). Conversely,aliens with no specialist herbivores did not present thistrend. Our results also provided partial support (in aliens)for the hypothesis that leaf phenolic contents would beaffected by N and P in different ways because of theirdifferent cellular metabolic processes (Wright et al., 2010).

Foliar Tta and TT contents were not related to any ofthose leaf economic traits in any of both groups of speciesnor to any of the main nutrients, N or P. Regarding themore evolutive hypotheses, the results partially support themodified EICA-related hypothesis (Joshi and Vrieling,2005; Stastny et al., 2005), which suggests that alienspecies have a larger content of low cost defenses such as

terpenes against generalist herbivores. These results alsodemonstrate, however, that aliens had not lost the capacityfor formation of high-carbon cost phenolics or tannins.

The different results of alien vs. native comparisons forTT, Tta, and TP contents also suggest a set of differentpossible physiological, ecological, and evolutionary roles ofthese different types of CBSC. The higher or lower contentof different chemical compounds does not depend only on adefense strategy. Other environmental factors such astemperature or drought could explain changes of secondarymetabolites contents such as terpenes since they are alsoinvolved in protection mechanisms in the face of abiotic(Peñuelas and Llusià, 2003, 2004; Peñuelas and Munné-Bosch, 2005; Lewis et al., 2006) and biotic (Viiri et al.,2001; Gershenzon and Dudareva 2007) stressors. Volatileterpenes also are involved in plant defense by multitrophicsignalling (Dicke and Baldwin, 2010).

In summary, the results show that alien species investless in structural defenses (they have lower LMA) but morein terpenes, which are low cost chemical defenses, effectiveat lower contents than other chemical defenses (Mote et al.,2007), and which strongly deter generalist herbivore attacks(Landau et al., 1994; Mote et al., 2007). Thus, the resultsare partly in accordance with the most recent “Evolution ofIncreased Competitive Ability” (EICA) hypothesis, whichproposes that lower cost defensive compounds are effectivein deterring generalist herbivores in the introduced range.However, the results are not in accordance with theexpected decreases in other high cost defense componentssuch as TP and Tta. These higher contents of lower costdefenses together with higher nutrient content and growthrates fit well with the fast-growing strategy of the alienspecies in resource rich areas such as the tropical islandswith old weathered soils where the plant invasive success isan emerging phenomenon.

Acknowledgements We thank Theodore Garland Jr. for providingmost of the statistical programs used for phylogenetic analyses. Thisresearch was supported by the University of Hawaii (G. P. Wilderresearch funds), and grants from the Spanish Government (CGL2006-04025/BOS, CGL2010-17172 and Consolider-Ingenio MontesCSD2008-00040), the Catalan Government (SGR 2009-458), theEstonian Ministry of Education and Science (grant SF1090065s07),the Spanish National Research council (CSIC-PIF08-006-3), and theEstonian Science Foundation (grant 7645).

J Chem Ecol (2010) 36:1255–1270 1263

Appendix

Table 1 Description of the study sites

Site Coordinates Average±SDa Average±SD precipitation(mm)

Average±SD annualtemperature (°C)

Species number

altitude (m) Annual Three driestmonths

Minimum Maximum Total Native Alien

Hahaione Valley 21°19’N, 157°43’W 390±140 1268±22 157±7 17.1±0.6 25.7±0.5 14 2 12

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

Tantalus 21°N, 20’157°49’W 441±24 3670±440 705±41 16.2±0.6 24.1±0.6 22 11 11

Wiliwilinui 21°19’N, 157°45’W 660±120 2100±150 413±60 15.2±0.9 23.8±0.8 25 22 3

a averages are based on the number of species sampled and species-specific locations. In statistical analyses, exact species-specific environmental data wereused

Table 2 Family, plant growth form, sampling sites in Oahu, Hawaii, characteristic ecological distribution, continent of origin and invasiveness ofall studied species

Speciesa Family Growth form Sampling siteb Speciesecology

Continentof origin

Invasi-venessc

Acacia confusa Fabaceae Tree St. Louis Heights dry-mesic Asia 3

Acacia koa Fabaceae Tree Wiliwilinui mesic-wet 0

Ageratina adenophora Asteraceae Herb Tantalus mesic-wet Americas 2

Alyxia stellata Apocynaceae Vine/Shrub Wiliwilinui mesic-wet 0

Antidesma platyphyllum Euphorbiaceae Tree Tantalus mesic-wet 0

Ardisia elliptica Myrsinaceae Shrub Hahaione Valley mesic-wet Asia 3

Bischofia javanica Euphorbiaceae Tree Tantalus mesic-wet Asia 2

Bobea elatior Rubiaceae Tree Wiliwilinui wet 0

Broussaisia arguta Hydrangeaceae Shrub Wiliwilinui wet 0

Buddleja asiatica Scrophulariaceae Shrub Wiliwilinui mesic-wet Asia 2

Carmona retusa Boraginaceae Shrub St. Louis heights dry-mesic Asia 1

Casuarina equisetifolia Casuarinaceae Tree St. Louis heights dry-mesic Australia 3

Cestrum nocturnum Solanaceae Shrub Tantalus wet Americas 3

Cheirodendron trigynum Araliaceae Tree Wiliwilinui wet 0

Cinnamomum burmannii Lauraceae Tree Tantalus mesic-wet Asia 2

Citharexylum caudatum Verbenaceae Shrub Tantalus mesic-wet Americas 3

Clermontia oblongifolia Campanulaceae Tree Tantalus wet 0

Clerodendrum macrostegium Verbenaceae Shrub Tantalus wet Asia 1

Coffea arabica Rubiaceae Shrub Tantalus mesic-wet Africa/Asia 2

Coprosma longifolia Rubiaceae Shrub Wiliwilinui mesic-wet 0

Desmodium incanum Fabaceae Shrub Hahaione Valley dry Americas 2

Diospyros sandwicensis Ebenaceae Tree Tantalus dry-mesic 0

Elaeocarpus bifidus Elaeocarpaceae Tree Tantalus and Wiliwilinui mesic-wet 0

Eucalyptus robusta Myrtaceae Tree St. Louis heights dry-mesic Australia 1

Falcataria moluccana Fabaceae Tree St. Louis heights dry-mesic Asia 2

Ficus macrophylla Moraceae Tree Hahaione Valley mesic-wet Australia 2

Ficus microcarpa Moraceae Tree St. Louis heights dry-mesic Asia 3

Freycinetia arborea Pandanaceae Vine/Shrub Tantalus wet 0

Haematoxylum campechianum Fabaceae Tree St. Louis heights dry Americas 2

Hedyotis acuminata Rubiaceae Vine/Shrub Tantalus mesic-wet 0

Hedyotis fosbergii Rubiaceae Shrub Wiliwilinui wet 0

1264 J Chem Ecol (2010) 36:1255–1270

Table 2 (continued)

Speciesa Family Growth form Sampling siteb Speciesecology

Continentof origin

Invasi-venessc

Hedyotis terminalis Rubiaceae Shrub Wiliwilinui mesic-wet 0

Heliocarpus americanus Malvaceae Tree Hahaione Valley dry-mesic Americas 1

Hibiscus arnottianus Malvaceae Tree Tantalus wet 0

Ilex anomala Aquifoliaceae Shrub Wiliwilinui wet 0

Ilex paraguariensis Aquifoliaceae Tree Tantalus mesic-wet Americas 1

Jasminum fluminense Oleaceae Vine St. Louis Heights dry-mesic Africa 2

Korthalsella complanata Santalaceae Mistletoe Wiliwilinui wet 0

Labordia tinifolia Loganiaceae Shrub Tantalus wet 0

Lantana camara Verbenaceae Shrub Hahaione Valley dry-mesic Americas 3

Mangifera indica Anacardiaceae Tree Tantalus mesic-wet Asia 1

Melaleuca quinquenervia Myrtaceae Tree St. Louis heights dry-mesic Australia 2

Melicope clusiifolia Rutaceae Shrub Wiliwilinui wet 0

Melicope peduncularis Rutaceae Shrub Wiliwilinui wet 0

Metrosideros macropus Myrtaceae Tree Wiliwilinui wet 0

Metrosideros polymorpha Myrtaceae Tree Hahaione Valley and Tantalus mesic-wet 0

Metrosideros rugosa Myrtaceae Shrub Wiliwilinui wet 0

Metrosideros tremuloides Myrtaceae Tree Tantalus mesic-wet 0

Myrsine lessertiana Myrsinaceae Shrub Wiliwilinui wet 0

Myrsine sandwicensis Myrsinaceae Shrub Wiliwilinui wet 0

Ochna thomasiana Ochnaceae Shrub Hahaione Valley dry Africa 1

Passiflora suberosa Passifloraceae Vine Wiliwilinui dry-mesic Americas 2

Persea americana Lauraceae Tree Tantalus series mesic-wet Americas 1

Pimenta dioica Myrtaceae Tree St. Louis heights dry Americas 1

Pisonia umbellifera Nyctaginaceae Tree Tantalus mesic-wet 0

Pluchea carolinensis Asteraceae Shrub Hahaione Valley dry-mesic Americas 2

Pouteria sandwicensis Sapotaceae Tree Tantalus mesic-wet 0

Psidium cattleianum Myrtaceae Tree Hahaione Valley mesic-wet Americas 3

Psidium guajava Myrtaceae Tree Hahaione Valley dry-mesic Americas 3

Rubus rosifolius Rosaceae Shrub Wiliwilinui wet Americas 2

Santalum freycinetianum Santalaceae Tree Wiliwilinui dry-mesic 0

Scaevola gaudichaudiana Goodeniaceae Shrub Wiliwilinui wet 0

Schinus terebinthifolius Anacardiaceae Tree Hahaione Valley dry-mesic Americas 3

Senna surattensis Fabaceae Tree St. Louis heights dry Asia/Australia 1

Sida fallax Malvaceae Shrub Hahaione Valley dry-mesic 0

Smilax melastomifolia Smilacaceae Vine Wiliwilinui mesic-wet 0

Stachytarpheta cayennensis Verbenaceae shrub Hahaione Valley dry-mesic Americas 3

Syzygium cumini Myrtaceae Tree Tantalus mesic-wet Asia 1

Syzygium sandwicensis Myrtaceae Tree Wiliwilinui wet 0

Tabebuia rosea Bignoniaceae Tree St. Louis heights dry-mesic Americas 1

Trema orientalis Ulmaceae Shrub Hahaione Valley dry-mesic Africa/Asia 2

Vaccinium calycinum Ericaceae Shrub Wiliwilinui wet 0

Wikstroemia oahuensis Thymelaeaceae Shrub Wiliwilinui mesic-wet 0

a Species nomenclature follows ARS/GRIN online database (USDA, ARS, National Genetic Resources Program. Germplasm Resources InformationNetwork - (GRIN), National Germplasm Resources Laboratory, Beltsville, Maryland, http://www.ars-grin.gov/cgi-bin/npgs/html/index.pl) and for Hawaiiannative species missing from this database (mainly Rubiaceae and Rutaceae) species nomenclature follows the Manual of the flowering plants of Hawai’i(Wagner et al., 1999)b Table 1 for the description of the study sitesc 0 – native species, 1 – low, 2 – moderate-high, 3 –high invasiveness

J Chem Ecol (2010) 36:1255–1270 1265

Tab

le3

Foliarcontentsof

totalph

enolics(TP),totaltann

ins(Tta)andtotalterpenes

(TT)andtheirrespectiv

eratio

srelativ

eto

leaf

NandPcontentforthestud

iednativ

eandalienspecies

Species

aSpecies

code

Origin

TotalPheno

lics

(TP)(m

gg-1)

TotalTann

ins

(Tta)(m

gg-1)

TotalTerpenes

(TT)(m

gg-1)

TP:N

(gg-1)

TP:P

(gg-1)

Tta:N

(gg-1)

Tta:P

(gg-1)

TT:N

(gg-1)

TT:P

(gg-1)

Acaciaconfusa

Ac

A10

1±12

20.9±9.9

n.d.

3.4±0.5

168.5+18

.80.70

6±0.352

35.0±11.8

n.d.

n.d.

Acaciakoa

Ak

N80

.5±10

.035

.7±2.7

n.d.

2.82

±0.10

66.4±1.3

1.26

±0.18

29.5±6.9

n.d.

n.d.

Ageratin

aad

enop

hora

Ag

A17

.4+4.0

n.a.

12.7±1.8.

0.553±0.04

07.2±5.4

n.a.

n.a.

4.03

±0.11

52.7±0.09

Alyxiastellata

As

N23

.0+5.3

2.09

±0.71

2.23

±0.12

48.1±3.4

0.20

3±0.011

4.8±0.2

n.d

n.d

Antidesmaplatyphyllu

mAp

N21

.6±3.5

2.50

±0.28

n.d.

1.00

+0.03

16.5+2.4

0.05

4±0.007

0.89

7±0.199

n.d.

n.d.

Ardisia

ellip

tica

Ae

A10

6±12

9.6±1.8

n.d.

7.13

±0.6

123+11

0.64

7±0.015

11.1±1.7

n.d.

n.d.

Bischofia

javanica

Bj

A55

.3±19

.97.77

±1.12

n.d.

3.94

±2.23

45.4±13

.00.55

4±0.037

6.39

±1.02

n.d.

n.d.

Bobea

elatior

Be

N43

.3±9.1

5.24

±1.8

n.d.

2.85

±0.24

75.7±7.7

0.38

9±0.110

10.3±3.9

n.d.

n.d.

Broussaisia

argu

taBa

N96

.9±8.0

15.8±4.2

n.d.

5.67

±0.11

114±13

0.86

4±0.242

17.4±4.6

n.d.

n.d.

Bud

dlejaasiatica

Bs

A42

.3±3.4

n.a.

n.d.

1.36

±0.20

32.0±6.2

n.a.

n.a.

n.d.

n.d.

Carmon

aretusa

Cr

A89

.3±5.0

2.10

±0.17

n.d.

2.99

±0.22

128±65

0.06

9±0.009

2.97

±1.07

n.d.

n.d.

Casuarina

equisetifolia

Ce

A24

.9±5.8

9.98

±1.17

n.d.

1.52

±0.13

59.4±7.4

0.611±0.072

23.8±2.7

n.d.

n.d.

Cestrum

nocturnu

mCn

A15

.0+4.1

2.39

±0.01

n.d.

0.504±0.20

17.35

±2.20

0.08

0±0.009

1.17

±0.03

n.d.

n.d.

Cheirod

endron

trigynum

Ct

N16

.0±1.4

1.78

±0.20

5.94

±1.60

1.07

±0.20

18.0±2.6

0.117±0.020

1.96

±0.30

3.96

±0.88

67.0±9.0

Cinna

mom

umbu

rmannii

Cb

A17

.1±1.4

3.45

±0.44

2.73

±1.31

0.838±0.01

220

.8±2.6

0.16

9±0.011

4.19

±0.69

1.33

±0.33

33.0±20

.0

Cith

arexylum

caud

atum

Ci

A29

.6±1.8

1.94

±0.12

n.d.

1.15

±0.01

19.7±5.3

0.07

3±0.008

1.26

±0.42

n.d.

n.d.

Clerm

ontia

oblongifo

liaCo

N16

.6±0.8

n.a.

n.d.

0.835±0.06

017

.1±0.3

n.a.

n.a.

n.d.

n.d.

Clerodend

rum

macrostegium

Cm

A22

.4±9.1

2.03

±0.05

n.d.

0.816±0.42

29.96

±5.61

0.07

3±0.013

0.88

5±0.195

n.d.

n.d.

Coffeaarabica

Ca

A23

.0+1.4

n.a.

n.d.

0.740±0.04

116

.7±1.7

n.a.

n.a.

n.d.

n.d.

Coprosm

along

ifolia

Cl

N41

.3±7.1

5.33

±2.02

n.d.

2.11

±0.33

46.1±5.2

0.26

9±0.058

5.87

±1.40

n.d.

n.d.

Desmodium

incanu

mDi

A35

.5±13

.3n.a.

n.d.

1.17

±0.08

26.1±12

.3n.a.

n.a.

n.d.

n.d.

Diospyros

sand

wicensis

Ds

N31

.9±8.1

15.2±2.9

n.d.

3.04

±0.09

45.0±13

.01.36

±0.24

20.0±4.0

n.d.

n.d.

Elaeocarpus

bifid

usEb

N12

9±75

1.45

±0.33

n.d.

11.0±0.7

240±17

00.03

8±0.020

0.90

±0.09

n.d.

n.d.

Eucalyptusrobu

sta

Er

A85

.6±14

.64.13

±0.54

1.06

±0.21

6.69

±0.59

91.3±10

.20.24

3±0.022

3.32

±1.01

0.83

1±0.050

11.3±1.3

Falcatariamoluccana

Fm

A87

.4±26

.914

.4±6.3

n.d.

3.25

±0.37

128±43

0.57

6±0.258

22.7±9.31

n.d.

n.d.

Ficus

macroph

ylla

Fa

A10

.1±0.7

1.71

±0.01

n.d.

0.596±0.05

010

.4±2.0

0.10

1±0.011

1.76

±0.08

n.d.

n.d.

Ficus

microcarpa

Fi

A53

.0±1.7

21.7±0

n.d.

3.61

±0.31

76.1±3.5

1.48

±0.34

31.2±6.9

n.d.

n.d.

Freycinetia

arborea

Fr

N14

.4±3.9

2.05

±0.24

n.d.

7.59

±0.30

11.7±4.5

0.10

4±0.019

1.61

±0.41

n.d.

n.d.

Haematoxylum

campechianum

Hc

A97

.3±24

.88.66

±0.80

n.d.

4.19

±0.59

115±22

0.112±0.007

3.06

±0.43

n.d.

n.d.

Hedyotis

acum

inata

Ha

N21

.3±4.3

15.0±13

.2n.d.

0.978±0.20

57.41

±1.20

0.68

7±0.550

5.21

±3.51

n.d.

n.d.

Hedyotis

fosbergii

Hf

N14

.2±2.4

1.90

±0.30

n.d.

0.776±0.08

014

.7±1.3

0.10

5±0.020

1.98

±0.62

n.d.

n.d.

Hedyotis

term

inalis

Ht

N25

.0±3.0

2.11

±0.12

n.d.

1.74

±0.04

31.2±11.7

0.14

6±0.013

2.62

±0.53

n.d.

n.d.

Heliocarpus

american

usHe

A61

.0±6.6

3.42

±0.62

0.123±0

.020

1.54

±0.01

36.7±5.6

0.09

0±0.022

2.14

±0.54

0.03

1±0.007

0.741±0.168

Hibiscusarnottianus

Hl

N16

.9±2.6

n.a.

n.d.

0.745±0.04

28.07

±1.16

n.a.

n.a.

n.d.

n.d.

Ilex

anom

ala

IaN

26.4±6.0

1.68

±0.22

n.d.

3.56

±0.90

68.9±20

.30.21

8±0.042

4.22

±0.65

n.d.

n.d.

Ilex

paragu

ariensis

IpA

11.4±3.0

2.00

±0.32

n.d.

0.402±0.12

011.5±5.3

0.07

0±0.011

1.98

±0.17

n.d.

n.d.

Jasm

inum

fluminense

JfA

18.0±2.1

2.02

±0.41

n.d.

0.920±0.27

914

.4±2.4

0.10

2±0.026

1.60

±0.20

n.d.

n.d.

1266 J Chem Ecol (2010) 36:1255–1270

Tab

le3

(con

tinued)

Species

aSpecies

code

Origin

TotalPheno

lics

(TP)(m

gg-1)

TotalTann

ins

(Tta)(m

gg-1)

TotalTerpenes

(TT)(m

gg-1)

TP:N

(gg-1)

TP:P

(gg-1)

Tta:N

(gg-1)

Tta:P

(gg-1)

TT:N

(gg-1)

TT:P

(gg-1)

Korthalsella

complan

ata

Kc

N10

.1±2.6

1.50

±0.22

n.d.

0.384±0.011

5.72

±2.61

0.05

5±0.006

0.81

9±0.097

n.d.

n.d.

Labordiatin

ifolia

Lt

N14

.7±1.0

n.a.

n.d.

0.813±0.03

611.6±3.2

n.a.

n.a.

n.d.

n.d.

Lantana

camara

Lc

A11.8±3.0

15.1±7.9

3.76

±0.60

0.421±0.02

24.24

±1.62

0.39

±0.0

3.44

±0.05

1.34

±0.39

13.5±3.1

Mangifera

indica

Mi

A80

.5±7.6

3.78

±0.19

0.138±0.00

15.03

±0.03

81.3±0.2

0.23

9±0.005

3.86

±0.24

0.08

7±0.015

1.40

+0.01

Melaleuca

quinquenervia

Mq

A27

.4±0.9

6.59

+2.32

16.2±1.1

2.58

±0.20

72.4±12

.90.60

9±0.171

17.1±6.0

15.2±0.0

428+1

Melicop

eclusiifolia

Mc

N33

.6±3.2

2.59

±0.13

5.12

±2.50

2.01

±0.41

35.1±4.6

0.15

4±0.023

2.69

±0.28

3.06

±3.21

53.4±49

.9

Melicopepeduncularis

Mp

N27

.1+0.3

2.80

±0.53

2.87

±0.39

1.76

±0.20

42.8±2.8

0.17

6±0.040

4.28

±0.89

1.87

±0.08

45.4±9.3

Metrosiderosmacropu

sMa

N17

8±1

2.21

±0.33

0.504±0.20

218

.2±1.4

394±30

0.22

9±0.013

4.96

±1.05

0.51

4±0.401

11.2±1.2

Metrosiderospo

lymorpha

Me

N78

.2±16

.33.16

±0.18

3.09

±0.90

6.59

±0.69

77.9±25

.80.27

3±0.003

3.22

±0.56

2.60

±0.20

30.7±3.9

Metrosiderosrugosa

Mr

N91

.3±9.0

6.25

±0.51

4.53

±2.00

9.41

±3.21

183±23

0.65

4±0.008

12.7±2.4

4.67

±2.38

91.0±50

.0

Metrosiderostrem

uloides

Mt

N73

.5±6.6

1.99

±0.20

0.240±0.09

05.73

±0.49

58.5±5.6

0.15

7±0.002

1.61

±0.17

0.18

7±0.070

1.92

±1.29

Myrsine

lessertia

naMd

N70

.1±11.0

12.2±3.9

4.03

±1.40

6.41

±0.10

110±13

1.12

±0.03

19.1±4.4

3.69

±0.29

63.2±7.7

Myrsine

sand

wicensis

Ms

N29

.3±8.4

5.00

±0.49

2.44

±1.22

2.64

±0.19

55.7±26

.80.51

4±0.010

10.9±2.1

2.20

±0.31

46.3±3.2

Ochna

thom

asiana

Ot

A20

.7±5.1

n.a.

n.d.

1.22

±0.30

27.8±11.5

n.a.

n.a.

n.d.

n.d.

Passiflo

rasuberosa

Pb

A17

.7±2.1

2.40

±0.33

n.d.

0.566±0.19

717

.0±6.3

0.07

6±0.002

2.27

±0.66

n.d.

n.d.

Perseaam

ericana

Pe

A61

.5±20

.147

.4±0.2

0.831±0.10

13.48

±1.10

74.4±22

.63.11

±0.80

66.5±6.5

0.47

0±0.089

10.1±0.8

Pimenta

dioica

Pd

A15

9±13

33.5±7.4

5.14

±2.41

11.7±1.0

354±48

2.46

±0.38

74.5±12

.03.59

±2.60

114±26

Pison

iaum

bellifera

Pi

N8.4±0.5

2.04

±0.05

n.d

0.245±0.01

95.74

±0.79

0.05

8±0.001

1.37

±0.08

n.d

n.d

Pluchea

carolin

ensis

Pc

A111±26

n.a.

0.192±0.09

74.04

±0.61

51.4±1.4

n.a.

n.a.

0.07

0±0.036

0.891±0.374

Pou

teriasandwicensis

Ps

N38

.5±11.4

3.92

±0.72

n.d

1.68

±0.22

41.6±17

.60.17

4±0.033

4.30

±1.11

n.d

n.d

Psidium

cattleianum

Pt

A72

.7±6.3

9.70

±6.50

6.66

±0.60

3.92

±0.53

68.2±5.1

0.51

8±0.182

9.02

±4.19

3.59

±0.20

62.5±9.4

Psidium

guajava

Pg

A89

.4±5.0

12.5±2.9

2.11

±0.69

7.43

±0.18

123±13

0.99

6±0.130

16.5±3.7

1.75

±1.11

29.0±26

.5

Rubus

rosifoliu

sRu

A73

.0±4.9

2.54

±0.52

2.35

±1.00

2.70

±0.80

85.1±18

.90.04

2±0.003

1.34

±0.40

0.86

8±0.311

27.4±21

.2

Santalum

freycinetia

num

Sf

N118±4

14.6±8.1

n.d

4.60

±0.42

121±33

0.57

0±0.289

15.0±12

.5n.d

n.d

Scaevola

gaudichaud

iana

Sg

N36

.8±3.0

1.87

±0.40

n.d

1.16

±0.04

51.7±5.0

0.06

3±0.020

2.81

±0.53

n.d

n.d

Schinusterebinthifoliu

sSt

A67

.2±4.6

n.a.

12.8±1.1

3.32

±0.20

43.2±4.0

n.a.

n.a.

6.30

±1.82

82.1±15

.5

Sennasurattensis

Se

A54

.2±22

.06.79

±2.33

n.d

2.05

±1.03

57.1±13

.20.27

6±0.053

7.69

±1.10

n.d

n.d

Sida

falla

xSi

N12

.2±3.5

n.a.

n.d

0.526±0.07

12.92

±0.81

n.a.

n.a.

n.d

n.d

Smila

xmelastomifo

liaSm

N29

.5±8.1

3.43

±1.37

n.d

2.58

±1.22

57.3±23

.70.29

6±0.101

6.58

±2.23

n.d

n.d

Stachytarpheta

cayennensis

Sh

A26

.6±9.0

n.a.

n.d

1.56

±0.03

15.4±5.0

n.a.

n.a.

n.d

n.d

Syzygium

cumini

Sc

A22

.4±3.9

2.80

±0.32

7.95

±0.82

1.13

±0.10

23.3±6.7

0.13

8±0.013

2.83

±0.55

4.03

±0.05

82.6±7.7

Syzygium

sandwicensis

Sy

N86

.7+17

.16.21

±1.90

0.284±0.04

06.92

±0.67

132±24

0.49

6±0.141

9.48

±2.67

0.22

6±0.050

4.32

±0.93

Tabebu

iarosea

Tr

A20

.8±3.3

2.88

±0.29

n.d

1.88

±0.09

40.2±8.6

0.26

0±0.028

5.56

±0.70

n.d

n.d

Trem

aorientalis

ToA

16.8±1.7

n.a.

n.d

0.513±0.05

17.05

±2.50

n.a.

n.a.

n.d

n.d

Vaccinium

calycinum

Vc

N67

.5±8.3

9.78

±1.83

n.d

5.58

±0.70

159±15

0.80

2±0.121

22.8±3.6

n.d

n.d

Wikstroem

iaoa

huensis

Wo

N59

.3±3.1

8.98

±1.01

n.d

3.47

±0.46

66.4±3.1

0.52

7±0.074

10.1±0.8

n.d

n.d

aSpecies

nomenclaturefollo

wsARS/GRIN

onlin

edatabase

(USDA.ARS.NationalGenetic

Resources

Program

.Germplasm

Resources

Inform

ationNetwork-(G

RIN).NationalGermplasm

Resources

Laboratory.

Beltsville.Maryland.

http://www.ars-grin.gov/cgi-bin/npgs/htm

l/index.pl)

andforHaw

aiiannativ

especiesmissing

from

this

database

(mainlyRubiaceae

andRutaceae)

speciesnomenclature

follo

wstheManualof

theflow

eringplantsof

Haw

aii(W

agneret

al.,19

99)

n.dno

tdetected.n.ano

availabledata

J Chem Ecol (2010) 36:1255–1270 1267

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