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Ecophysiological plasticity and local differentiation help explainthe invasion success of Taraxacum officinale (dandelion) inSouth America

Marco A. Molina-Montenegro, Claudio Palma-Rojas, Yulinka Alcayaga-Olivares, Rómulo Oses,Luis J. Corcuera, Lohengrin A. Cavieres and Ernesto Gianoli

 M. A. Molina-Montenegro (marco.molina@ceaza.cl) and Y. Alcayaga-Olivares, Centro de Estudios Avanzados en Zonas Áridas (CEAZA),Facultad de Ciencias del Mar, Univ. Católica del Norte, Larrondo 1281, Coquimbo, Chile. MAM-M also at: Depto de Botánica, Univ.de Concepción, Casilla 160-C, Concepción, Chile. – C. Palma-Rojas and E. Gianoli, Depto de Biología, Univ. de La Serena, Casilla 554,La Serena, Chile. EG also at: Depto de Botánica, Univ. de Concepción, Casilla 160-C, Concepción, Chile. – R. Oses, Inst. de Investigaciones

 Agropecuarias (INIA), Centro Regional Intihuasi, La Serena, Chile. – L. J. Corcuera and L. A. Cavieres, Depto de Botánica, Univ. de Concepción,Casilla 160-C, Concepción, Chile. LAC also at: Inst. de Ecología y Biodiversidad (IEB), Santiago, Chile.

Plasticity and local adaptation have been suggested as two main mechanisms that alien species use to successfully tolerateand invade broad geographic areas. In the present study, we try answer the question if the mechanism for the broad dis-tributional range of T. o ffi cinale  is for phenotypic plasticity, ecotypic adaptation or both. For this, we used individuals ofT. o ffi cinale   originated from seeds collected in five localities along its latitudinal distribution range in the southern-hemisphere. Seedlings were acclimated at 5 and 25C for one month. After the acclimation period we evaluated ecophys-iological and cytogenetic traits. Additionally, we assessed the fitness at each temperature by recording the seed output ofindividuals from diff erent localities. Finally, we performed a manipulative experiment in order to assess the tolerance toherbivory and competitive ability between T. o ffi cinale  from all origins and Hypochaeris scorzonerae  a co-occurring nativespecies. Overall, individuals of T. o ffi cinale  showed high plasticity and ecotypic adaptation for all traits assessed in thisstudy. Changes both in physiology and morphology observed in T. o ffi cinale  from diff erent origins were mostly correlated,

enhancing their ecophysiological performance in temperatures similar to those of their origin. Additionally, all localitiesshowed the same chromosome number and ploidy level. On the other hand, all individuals showed an increase theseed output at 25C, but those from northern localities increased more. T. o ffi cinale  from all origins was not significantlya ff ected by herbivory while native showed a negative eff ect. On the other hand, T. o ffi cinale  exerted a strong negativeeff ect on the native species, but this former not eff ected significantly to the invasive T. o ffi cinale . High plasticity andlocal adaptation in all ecophysiological traits, seed-set and the low cytogenetic variability in T. o ffi cinale   suggests thatboth strategies are present in this invasive plant species and are not mutually exclusive. Finally, higher tolerance to her-bivory and competitive ability suggests that T. o ffi cinale   could perform successfully in environments with diff erentclimatic conditions, and thus colonize and invade South-America.

 Alien invasive plants are those spreading beyond their origi-nal distribution range (Rejmánek et al. 2005), and giventhat a number of alien invasive plant species are colonizingbroad geographical areas, several studies have focused on thestrategies that enable their spread (Schweitzer and Larson1999, Sexton et al. 2002, Parker et al. 2003, Maron et al.2004, Geng et al. 2007, Molina-Montenegro et al. 2011,2012). Phenotypic plasticity and ecotypic diff erentiationare two of the main mechanisms by which widely distrib-uted plant species successfully tolerate environmental chal-lenges and colonize large areas (Joshi et al. 2001, Sextonet al. 2002, Parker et al. 2003, Richards et al. 2006, Genget al. 2007, Matesanz et al. 2010, Pichancourt and vanKlinken 2012). Phenotypic plasticity and ecotypic diff er-entiation are not mutually exclusive (Platenkamp 1990,Counts 1992, Andersson and Shaw 1994, Sexton et al. 2002,

Maron et al. 2004); both mechanisms contribute to the dis-tribution and abundance of plant species across environ-mentally heterogeneous ranges (Galen et al.  1991, Joshiet al. 2001, Santamaría et al. 2003, Molina-Montenegroet al. 2010, Molina-Montenegro and Naya 2012). Plasticitymay initially allow introduced species to become natural-ized across a range of environments (Sexton et al. 2002,Palacio-López and Gianoli 2011) and then heritablephenotypes may respond to local selection pressures, thusforming ecotypes better adjusted to local conditions (Sextonet al. 2002).

Studies evaluating the role of plasticity and ecotypic dif-ferentiation in the success of plant establishment have oftenfocused on morphological traits (Counts 1992, Santamaríaet al. 2003, Dorken and Barrett 2004, Gianoli 2004,Limousin et al. 2012, Pichancourt and van Klinken 2012).

Ecography 36: 718–730, 2013doi: 10.1111/j.1600-0587.2012.07758.x 

© 2012 e Authors. Ecography © 2012 Nordic Society OikosSubject Editor: Francisco Pugnaire. Accepted 9 October 2012

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Plant physiological plasticity and tolerance to herbivory,being important traits for plant adaptation to novel environ-ments, have received less attention in such studies (but see

 Williams et al. 1995, He and Dong 2003, Parker et al.2003). Physiological traits that control carbon uptake and

 water loss are highly plastic (Sage 1994, Heschel et al. 2004,Saldaña et al. 2005) and are key determinants of growth andreproduction (Ackerly et al. 2000, Gianoli et al. 2012).Tolerance to herbivory refers to the ability of a plant to

maintain its fitness despite tissue loss to herbivores (Straussand Agrawal 1999) and may play a role in facilitating asuccessful invasion (Murren et al. 2005, Stastny et al. 2005).Physiological performance and herbivory, through theireff ects on plant fitness, may play a significant role in habitatcolonization along environmental gradients.

It has been suggested that exotic species gain a competi-tive edge over natives because of their ability to exploitresources unavailable (or less available) to natives (Macket al. 2000). A recent meta-analysis concluded that wide-spread alien plants are better able to capitalize on increasedresource availability (Dawson et al. 2012). Changes inbiomass in both natives and exotics have been used as a

proxy to test their reciprocal competitive eff ects (Maronand Marler 2008). Phenotypic plasticity in morphologicaland/or physiological traits may grant plant success viaincreased resource capture, which would be reflected inchanges in biomass. Considering that climatic heterogene-ity increases with latitude (Gaston and Chown 1999,Molina-Montenegro and Naya 2012), and that the expres-sion of plant phenotypic plasticity is positively associated

 with environmental heterogeneity (Gianoli 2004, Gianoliand González-Teuber 2005, Baythavong and Stanton 2010,Molina-Montenegro et al. 2010), plants from populationslocated at higher latitudes are expected to show greaterplasticity. Alternatively, plastic responses in plants at higher

latitudes could not be of greater magnitude if costs of

plasticity, which constrain its expression (van Kleunen andFischer 2005, Valladares et al. 2007), are more significant instressful environments.

Taraxacum o ffi cinale  (dandelion) is a worldwide distrib-uted species native to Europe (Fig. 1). It is consideredone of the most aggressive invasive plants around the

 world (Holm et al. 1997). Taraxacum o ffi cinale   is foundgrowing in disturbed and undisturbed sites in wide altitu-dinal and latitudinal gradients (Molina-Montenegro and

Cavieres 2010, Molina-Montenegro and Naya 2012). InSouth America it has a long latitudinal distributionalrange, from Colombia (12N) to Tierra del Fuego inChile (54S), spanning hot-wet and dry-cold habitats(Molina-Montenegro and Naya 2012). It grows from sealevel to 3600 m in the Andes of central Chile. Despite itsremarkable distribution range and aggressive weed status,little is known about the physiological mechanisms thatenable T. o ffi cinale   to be successful in such a wide varietyof habitats. In the present study we address phenotypicplasticity and ecotypic diff erentiation as possible explana-tions for the broad distributional range of T. o ffi cinale .

 We studied morphological, physiological, reproductive

and cytogenetic traits in individuals of T. o ffi cinale   grownfrom seeds collected in five localities along its latitudinaldistribution range in South America. Specifically, we evalu-ated the occurrence of plastic and ecotypic responses ingas exchange traits, chlorophyll fluorescence, freeze toler-ance, and shoot morphology in plants exposed to two tem-peratures. Additionally, we evaluated seed production andploidy level in plants growing at temperatures similar tothose found at the extremes of the distribution gradient of  T. o ffi cinale   in South America. We also performed twomanipulative experiments in order to assess whether thenegative eff ects of simulated herbivory and inter-specificcompetition was greater in T. o ffi cinale   than in a closely

related native species.

Figure 1. Taraxacum o ffi cinale population growing in the field in southern Chile. Photographed by Alejandra Lafon in March 2009.

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Material and methods

Seed collection and growth conditions

Seeds of Taraxacum o ffi cinale  were collected in five localities:Manta (Ecuador), Trujillo (Perú), and La Serena, Valdiviaand Punta Arenas (Chile). is latitudinal gradient coversfrom ca 0 to ca 54S, including a significant thermic gradi-ent (Fig. 2, Table 1). All seeds were collected at sea level,

to reduce altitudinal eff ects (Fig. 2). A small number of seeds (four to five) per individual

plant collected from a relatively large number of sampled

plants (40–45) per population provided the initial pool ofseeds. As T. o ffi cinale   has apomictic reproduction (Va ut2003), samples were taken from widely separated plants toavoid sampling the same genet twice. Seeds in each locality

 were collected from three populations separated by approxi-mately 1 km each. All seeds collected in the three popula-tions of each locality were pooled and randomized beforesorting them into experimental treatments. Seeds fromall localities were germinated in a room at 24 2C on wet

filter paper in Petri dishes and planted in 300-ml plasticpots filled with potting soil. First generation plants (F1) weregenerated from this initial seed pool and were grown in a

Figure 2. Geographic location of the populations of Taraxacum o ffi cinale   used in the study. e elevation, latitude and longitude ofeach locality where the seeds were collected are shown.

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greenhouse at Univ. de Concepción, Concepción (3648S,7303 W) under natural conditions of light and temperature(1300 mol m2  s1  50 and 22 2C, respectively).ese plants were also put in 300-ml plastic pots filled

 with potting organic soil and watered daily with 75 ml of tap water. After five months these plants produced the achenesthat were used to obtain experimental plants (F2).

Seedlings from all localities were planted in 300-mlplastic pots filled with potting soil. One week after theappearance of the first true leaf, seedlings were transferred togrowth chambers (Forma Scientific) with a photon fluxdensity (PFD) of 170 mol m2 s1 and 16/8 h light/dark

photoperiod. e two temperature treatments consistedof transferring 40 individuals from each locality describedabove to a growth chamber set at either 5C or 25C for90 d. ese temperatures were chosen because they areclose to the mean temperatures in each extreme of the latitu-dinal gradient (Table 1). Plants at 5C and 25C were irri-gated daily with 50 and 75 ml tap water, respectively.

 All plants were supplemented with Phostrogen (Solaris,NPK, 14:10:27) using 0.2 g l1 once every 15 d. Plastic potspositions were randomized within the experimental plotevery five days and interpot distances were sufficient to pre-vent mutual shading. Germination percentage (ANOVA,F4, 296  117.3, p 0.89) and phenology (63 9 d for Pta.

 Arenas and 71 6 d for Trujillo) were similar betweenindividuals from diff erent populations.

Physiological performance

 After 90 d of temperature acclimation, ten individualsfrom each locality at 25C and another ten at 5C weretaken for fluorescence measurements at room temperature.Fluorescence signals (Maxwell and Johnson 2000) weregenerated by a pulse-amplitude modulated fluorometer(FMS 2, Hansatech, Instruments, Norfolfk, UK). Onefully-developed attached leaf from each individual wasdark-adapted for 30 min (to obtain open PSII centers)using leaf-clips to ensure maximum photochemical effi-ciency. e optic fiber and its adaptor were fixed to a ringlocated over the clip at approximately 10 mm from thesample and the diff erent light pulses were applied (seebelow). Signal recordings and calculations were performedusing the data analysis and control software provided withthe instrument. Minimal fluorescence (F0) with all PSIIreactions in the open state was determined by applyinga weak modulated light (0.4 mol m2  s1). Maximumfluorescence (Fm) with all PSII reaction centers in theclosed state was induced by a 0.8 s saturating pulse of

 white light (9000 mol m2  s1). After 15 s, the actinic

light (180 mol m2 s1) was turned on and the same satu-rating pulse described previously was applied every 60 suntil steady-state photosynthesis was reached, in order toobtain Fs and Fm. Finally, F0 was measured after turningoff   the actinic light and applying a 2 s far red light pulse(Pérez-Torres et al. 2004).

e same ten individuals used for fluorescence wereselected for gas exchange measurements. One expanded leaf

 was used for each individual for gas exchange measurement with a fully portable infra-red gas analyzer (CIRAS-2,PP-Systems Haverhill, MA). A single leaf was insertedinto the Parkinson leaf cuvette of the IRGA, where net pho-

tosynthesis and stomatal conductance were registered. Allmeasurements were performed at midday, with photosyn-thetic active radiation (PAR) intensity provided by instru-ment (1200 mol m2  s1) and at room temperature(20 2C).

Thermal analysis

One expanded leaf with the apex removed was selected inseven diff erent individuals from each population andeach temperature treatment. Each leaf was attached to athermocouple (Copper-constantan, Gauge 30; Cole Palmer

Instruments, Vernon Hills, IL, USA) and immediatelyenclosed in a small, tightly closed cryotube to avoid changesin tissue water content. Temperature was continuouslymonitored and recorded (1 measurement per s) with an ACjrdata acquisition board connected to a multi-channel tem-perature terminal panel (Strawberry Tree, Sunnyvale, CA,USA). e tubes were placed in a cryostat and the tem-perature was lowered from 0 to 15C at a rate of approxi-mately 2C h1. e temperature at the initiation of thefreezing exotherm corresponds to the ice nucleation tem-perature, while the highest point of the exotherm representsthe freezing temperature of the water in the apoplast(including symplastic water driven outwards by the water

potential diff erences caused by apoplastic ice formation)(Larcher 1995, Bravo et al. 2001).

Shoot measurements

 After the acclimation treatment, ten individuals fromeach locality were selected and the following traits weremeasured: leaf width and length (mm) and leaf dry biomass(mg, mean of three oldest fully-expanded leaves of eachindividual from each locality oven-dried for 72 h at 70C).

 All measurements were performed with a digital caliper(Mitutoyo Corporation; resolution 0.01 mm).

Table 1. Monthly and annual mean temperature ( 2 SE) in the sites where the seeds of Taraxacum officinale were collected. Data wereobtained from The Weather Channel ( www.weather.com).

Locality Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Mean

Manta 26 26 29 26 26 25 24 24 24 24 24 26 25.3 ( 0.9)Trujillo 21 22 22 21 20 19 18 17 17 18 18 19 19.3 ( 1.1)La Serena 17 17 16 14 12 11 11 11 12 13 14 16 13.7 ( 1.4)Valdivia 16 15 13 11 9 7 7 7 9 11 13 15 11.1 ( 1.9)Pta. Arenas 11 9 9 7 4 2 2 3 5 7 8 10  6.6 ( 1.9)

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 We also performed an experiment of tolerance of her-bivory in 20 individuals of T. o ffi cinale   from all sites and20 individuals of H. scorzonerae . Two-months-old damagedplants suff ered 25% defoliation with scissors (50% of leafarea removed in half the leaves; leaves were clipped alongthe mid-vein). We selected this kind of damage because it iscommonly found in the field for these species (Molina-Montenegro unpubl.). Half the plants were subjected toartificial leaf damage (25% defoliation) and half served as

controls (n 10 plants per treatment). One day after inflict-ing leaf damage, we recorded the photochemical efficiency(Fv/Fm) as described above. e number of heads produced

 was recorded every 3 d in all individuals.

Statistical analysis

In order to test the main hypothesis of this study, i.e. whetherperformance patterns of Taraxacum o ffi cinale  along a broadlatitudinal gradient reflect either phenotypic plasticity orecotypic diff erentiation, a two-way ANOVA was applied.Main factors were origin and temperature, and ecophysio-logical traits were the response variables. When factors

 were significant, diff erences in the mean of each ecophysio-logical trait were evaluated between populations with a Tukeytest. Phenotypic plasticity will be inferred if the tempera-ture factor is significant, and ecotypic diff erentiation willbe proved if the origin turns to be a significant factor. A sig-nificant interaction of factors will imply the occurrence ofpopulation diff erentiation in plasticity. Likewise, valuesof seed output per capitulum were averaged for eachT. o ffi cinale  individual, and this value was compared by two-

 way ANOVA between T. o ffi cinale   individuals growing at5 and 25C and from each origin. Inspection of these fitnessresults will improve the interpretation of the first results(plasticity vs diff erentiation).

Similarly, we compared by two-way ANOVA the com-petition experiment and the eff ects of simulated herbivory.Comparisons between native and invasive species were con-ducted separately for each temperature because the aim ofthis study was to compare the competitive strengthof the native and the invasive species growing under twotemperatures rather than to evaluate the eff ect of tempera-ture on native-invasive relationships. For all ANOVAs, theassumptions of normality and homogeneity of variances

 were tested using the Shapiro–Wilks and Bartlett tests,respectively (Zar 1999).

ResultsPhysiological performance

Maximum photosynthetic efficiency (Fv/Fm) increased with temperature in all localities (Fig. 3A). e origin factor was also significant (Table 2). e Tukey test showed thatManta and Trujillo form a group with lower Fv/Fm than asecond group conformed by La Serena, Valdivia and Punta

 Arenas (Fig. 3A). Additionally, the analysis did not showsignificant diff erences within these groups (Table 3). einteraction between origin and temperature was significant(Table 2). Although the maximum photosynthetic efficiency

Seed output

To assess the eff ects of temperature on seed output, F2seedlings from each origin were chosen and transferred to

 walking growth chambers (Forma Scientific) with a photonflux density (PFD) of 200 mol m2 s1 and 16/8 h light/dark photoperiod set at 5C or 25C for 100 d and irrigateddaily and supplemented with Phostrogen (Solaris, NPK,14:10:27) using 0.2 g l1 once every 15 d.

 When capitula were closed indicating that seeddevelopment had begun, they were bagged with nylon-meshbags to prevent seed loss. Bagged capitula were collectedand seed output was calculated as the ratio between thenumber of fully filled seeds and the total number of seeds(i.e. including aborted and predated seeds) produced percapitulum.

Cytogenetic analysis

Roots of germinated seeds from each locality were pre-treated with colchicine 0.05% (w/v) at 18C for 3 h, fixed inethanol-glacial acetic acid (3:1 v/v) at 4C for 24 h, andstored in ethanol 70% (v/v) at 4C. To determine chromo-some number, roots tips were stained with the Feulgen reac-tion and chromosome preparations were made by squashingroot meristems (Palma-Rojas et al. 2007).

Interspecific competition and tolerance of herbivory

 We evaluated competition between the exotic Taraxacumo ffi cinale  from diff erent origins along the latitudinal gradientand the native Hypochaeris scorzonerae , both members of the

 Asteraceae tribe Lactuceae. Both species co-occur alonga fraction of the latitudinal gradient considered here, and

show similar morphology and life history traits. For example,both species have leaves in rosettes at the soil level, showyyellow heads and its seeds are mainly dispersed by wind(Matthei 1995). Seeds of H. scorzonerae   (four to five perindividual plant) were collected from a relatively largenumber of sampled plants (60–65) in La Serena and weregerminated in a room with filter paper in Petri dishes asdescribed above for T. o ffi cinale .

 We calculated the relative competition intensity index(RCI; Grace 1995) between T. o ffi cinale   (To) andH. scorzonerae  (Hs ) under two temperatures (5C and 25C)inside of growth chambers (same conditions as describedabove). To assess the competitive eff ect, 20 individuals ofeach species – and origin for T. o ffi cinale  – were grown alone(monoculture) and 10 individuals of each origin of T.o ffi cinale  were grown with 10 individuals of H. scorzonerae  (one pair per pot of 500-ml 10 pots per situation) at twoexperimental temperatures. We focused on the outcomeof competition between the invasive and the native speciesusing final biomass (Bsp) as response variable. us, weassessed the competitive impact of Taraxacum from diff er-ent origins on the native species (RCIHs   [BHs   Mono-culture BHs Taraxacum]/BHs   Monoculture), and theresistance of the native species to invasion by assessing itsimpact on Taraxacum  (RCITo  [BTo  MonocultureBTo Hypochaeris ]/BTo Monoculture).

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 Arenas increased even more (Table 3; Fig. 3B). Similarly

to the net photosynthesis rate, stomatal conductancealso increased significantly with temperature (Table 2);also, stomatal conductance was diff erent between localities(Table 2). e interaction factor between temperature andorigin proved to be significant, because although in alllocalities the stomatal conductance increased with tempera-ture, in Manta and Trujillo showed a greater increase, caus-ing crossed reaction norms (Fig. 3C).

Table 2. Two-way ANOVA of the effects of origin (O) and tempera-ture (T) on maximum efficiency of photosystem II (Fv/Fm), netphotosynthesis rate (Pn), stomatal conductance (g), ice nucleationtemperature (INT), leaf width (LW), leaf length (LL) and dry mass(DM) in Taraxacum officinale  individuals from Manta, Trujillo,La Serena, Valdivia and Punta Arenas, after 90 d of acclimation at5 or 25C.

Trait F p

Fv/FmOrigin 5.1    0.041Temperature 1308.8    0.001O T 34.3    0.029

PnOrigin 312.2 0.012Temperature 7161.2    0.001O T 98.1 0.011

gOrigin 5.5 0.003Temperature 1034.3    0.001O T 25.9    0.001

INTOrigin 5.0    0.014Temperature 8.9 0.042O T 8.8    0.001

LWOrigin 9.5 0.002Temperature 38.8    0.001O T 3.7 0.018

LLOrigin 129.6    0.001Temperature 113.4    0.001O T 37.1    0.001

DMOrigin 741.5    0.001Temperature 431.1 0.009O T 29.5 0.012

Table 3. Analysis a posteriori of ecophysiological traits in Taraxacumofficinale individuals from Manta (MA), Trujillo (TR), La Serena (LA),Valdivia (VA) and Punta Arenas (PA) localities after 90 d of acclima-tion at 5 and 25C. Significant differences between localities aredenoted with different letters.

5C 25C

Traits MA TR LA VA PA MA TR LA VA PA

Fv/FmNet

photosynthesisStomatal

conductanceIce nucleation

temperatureLeaf widthLeaf lengthDry mass

BB

C

B

BBC

BB

BC

A

CCD

AA

B

AB

AABB

AA

A

B

BAA

AA

A

A

AAB

BE

A

A

ABC

AD

A

B

BCC

BC

B

B

ABB

BB

B

B

ABA

CA

B

A

ABA

BCSeed output A A B BC CD DE E E E E

Figure 3. (A) photochemical efficiency of photosystem II (Fv/Fm),(B) net photosynthesis rate, and (C) stomatal conductance inTaraxacum o ffi cinale  individuals from Manta (MA), Trujillo (TR),La Serena (LA), Valdivia (VA) and Punta Arenas (PA). Mean values( 2 SE) in physiological parameters after 90 d of acclimation at5 and 25C are shown.

(Fv/Fm) increased with temperature in all localities, inthe Manta and Trujillo localities the increase was greater(Fig. 3A).

Net photosynthesis rate was significantly higher at25C than at 5C in all localities (Table 2). e analysisshowed significant diff erences in the net photosynthesis rateamong diff erent localities, demonstrating again the presenceof two groups (Table 3; Fig. 3B). e interaction factorbetween temperature and localities also was significant.

 Although all localities increased their net photosynthesisrates with temperature, La Serena, Valdivia and Punta

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level to be triploid in all of them (Fig. 7). Additionally, allchromosomes showed a similar size among diff erent locali-ties (Fig. 7).

Competition and tolerance of herbivory

Taraxacum o ffi cinale   from all sites showed higher successthan native species. e relative competition intensity index

(RCI) showed that T. o ffi cinale   from all latitudes exertedstrong competitive eff ects on H. scorzonerae , depressing itsbiomass from 65 to 34% at 25C and from 48 to 33%at 5C (Fig. 8). In contrast, native plants showed a weakeff ect on T. o ffi cinale , which showed from 36 to11% increasein biomass at 25C and a increase in biomass from 21to 14% at 5C (Fig. 8). Additionally, T. o ffi cinale   fromnorthern localities (Manta and Trujillo) had greater negativeeff ects on biomass of the native species, being this eff ecthigher at 25C than at 5C (F4, 90  57.76, p 0.001and F1, 90  107.16, p 0.001, respectively, Fig. 8). Onthe other hand, those individuals of T. o ffi cinale   fromsouthern localities (Valdivia and Pta. Arenas) grown with

H. scorzonerae   individuals significantly increased their bio-mass more than those from northern sites at 5C, whileat 25C those T. o ffi cinale  individuals from northern locali-ties (Manta and Trulillo) produced significantly higherbiomass than those from southern populations (Fig. 8).

Overall, simulated herbivory decreased significantlythe physiological performance (Fv/Fm; F5, 108  10.20,p 0.001) and flower production (F5, 108  8.31, p 0.001)compared with control both at 5C and 25C (Fig. 9).Nevertheless, only for native species the treatment of simu-lated herbivory a ff ected negatively and significantly theseresponses, being this decrease of 66 and 67% for Fv/Fmand a decrease of 77 and 65% for flower production at 5Cand 25C, respectively (Fig. 9).

(Fig. 6); this diff erence was statistically significant (F1, 110 

 1430.21, p 0.001). Individuals from southern originsshowed significantly greater seed output (F4, 110   50.7,p 0.001) than those from Manta and Trujillo (Fig. 6).On the other hand, the interaction eff ect was significant(F4, 110  71.1, p 0.001); although individuals from allorigins showed high values of seed output at 25C, thosefrom Manta and Trujillo decreased more at low temperature(Fig. 6).

Cytogenetic analysis

e chromosome number in all Taraxacum o ffi cinale  individuals from five localities was 24, revealing the ploidy

Figure 6. Seed output in Taraxacum o ffi cinale   individuals accli-mated for 90 d at 5 and 25C, from Manta (MA), Trujillo (TR),La Serena (LA), Valdivia (VA) and Punta Arenas (PA). Mean values( 2 SE) at are shown.

Figure 7. Metaphase plates in meristematic cells of Taraxacum o ffi cinale  individuals from Manta (A), Trujillo (B), La Serena (C), Valdivia(D) and Punta Arenas (E). All individuals analyzed from five populations have 24 chromosomes. Bar: 10 .

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latitudinal gradient. Moreover, our analysis also detecteddiff erentiation in plastic responses. Changes in both physi-ology and morphology observed in T. o ffi cinale  were mainlycorrelated to enhance their performance in the environ-ments similar to the origin. ese results suggest thatecotypic diff erentiation and phenotypic plasticity arenot mutually exclusive mechanisms for the successfulestablishment of T. o ffi cinale  along the latitudinal gradient(Joshi et al. 2001). Several studies have shown that greater

morphological plasticity and ecotypic diff erentiation inresponse to environmental conditions, including herbivores(Schierenbeck et al. 1994), and enhanced carbon uptake(Schierenbeck and Marshall 1993), may influence the suc-cess of plant invasion (Maron et al. 2004, Nagel andGriffin 2004).

Photochemical efficiency of photosystem II (Fv/Fm) inT. o ffi cinale  individuals from all localities was greater at thehigher temperature of acclimation. is suggests that theperformance of photosystem II shows a plastic response.Similarly, in leaves of Secale cereale  (winter rye), which natu-rally grows at ca 25C, Fv/Fm decreased nearly 15%

 when they were cold acclimated at 5C (Boese and Huner

1990). It has been suggested that plasticity in some traitsthat improve the Fv/Fm responses could help explain thespread in an invasive Mediterranean plant species (Travesetet al. 2008). On the other hand, net photosynthesis andstomatal conductance decreased substantially after coldacclimation in all the localities sampled. ese resultssuggest an inhibition of photosynthetic capacity in plantsafter cold acclimation (Holaday et al. 1992, Brüggemannet al. 1994, Hurry et al. 1995). Gas exchange measurementsin T. o ffi cinale  revealed both plastic and ecotypic responses.Nagel and Griffin (2004), working with the invasive speciesLythrum salicaria , showed that this plant species assimilated208% more carbon per unit of energy invested in leaf

biomass than either of the co-occurring native species, sug-gesting that an increase in carbon uptake may influenceits invasive success. On the other hand, Horton et al.(2010) reported that the invasive species Miscanthus sinensis  shows a rapid induction in photosynthetic parametersalong a luminic gradient, indicating that a high photosyn-thetic rate allows greater carbon gain than native plants.Our results suggest that T. o ffi cinale  is capable to adjust itsphysiological performance in such a way that resources areused efficiently in diff erent abiotic conditions along thelatitudinal gradient of distribution.

In the thermal analyses, only the locality of Mantadecreased the temperature at which apoplastic ice is formed

in tissue after cold acclimation, suggesting increased freezeresistance. In the other localities ice nucleation temperature was not a ff ected by cold acclimation. Moreover, only indi-viduals from the Manta population showed an incrementin the capacity to tolerate apoplastic ice formation aftercold acclimation. is is a somewhat surprising result, con-sidering that Manta plants originally developed in a tropicalclimate. Cold stress is a selective factor that acts overlongtime-scales and hence it may be assumed that localitiesin cold environments have undergone genetic differen-tiation rather than plasticity, allowing them to adapt theirfunctioning to local conditions (Körner 2003). Nevertheless,

 we cannot rule out the possibility that the cold tolerance

Figure 8. Manipulative competition experiment between thenative Hypochaeris scorzonerae  (empty bars) and individuals of theinvasive Taraxacum o ffi cinale  (black bars) from all origins. Shown isthe change in the biomass of the native and invasive speciesgrowing in monoculture and together in both at 5 and 25C treat-ments. Mean values SD are shown. Diff erent letters indicatesignificant diff erences; Tukey test,   0.05.

Discussion

It has been suggested that reproductive traits as high seedoutput, high germination rate and apomictic reproduction

 will favor the establishment success of alien species(Heywood 1989, Py šek 1997, Mullin 1998). Although

high reproductive success reflects an enhanced physiologi-cal functioning in a given environment, the physiologicalmechanisms associated with a high performance in alienplants are rarely found in the literature (Williams et al. 1995, Nagel and Griffin 2004, Molina-Montenegro et al.2012). Few studies on alien species along large geographicalgradients have addressed the mechanistic basis of theirsuccess, and very few have determined whether they areadapted by plastic or ecotypic responses (or both) in func-tional and fitness-related traits.

Overall, our results show both phenotypic plasticityand ecotypic diff erentiation for all ecophysiological traitsand fitness in T. o ffi cinale   populations from the studied

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plasticity and ecotypic diff erentiation in ecophysiologicaltraits are one of the main mechanisms that allow this speciesto spread along wide environmental gradients.

 Acknowledgements –  We thank Valeria Neira and Alexis Estay fortheir assistance in the laboratory analysis. anks to the NationalSeed Bank of Chile managed by INIA-Intihuasi (Vicuña, Chile)for initial seed pool of the native Hypochaeris scorzonerae  used inthis study.

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 We found that T. o ffi cinale  plants subjected to simulatedherbivory were not significantly a ff ected in their physio-logical performance and/or flower production, thus showinggreater tolerance of herbivory than plants from the co-occurring native species H. scorzonerae . Earlier studies have

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