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Ecophysiological plasticity and local differentiation help explain the invasion success of Taraxacum officinale (dandelion) in South 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 tolerate and invade broad geographic areas. In the present study, we try answer the question if the mechanism for the broad dis-tributional range of T. officinale is for phenotypic plasticity, ecotypic adaptation or both. For this, we used individuals of T. officinale originated from seeds collected in five localities along its latitudinal distribution range in the southern-hemisphere. Seedlings were acclimated at 5 and 25°C 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 of individuals from different localities. Finally, we performed a manipulative experiment in order to assess the tolerance to herbivory and competitive ability between T. officinale from all origins and Hypochaeris scorzonerae a co-occurring native species. Overall, individuals of T. officinale showed high plasticity and ecotypic adaptation for all traits assessed in this study. Changes both in physiology and morphology observed in T. officinale from different origins were mostly correlated, enhancing their ecophysiological performance in temperatures similar to those of their origin. Additionally, all localities showed the same chromosome number and ploidy level. On the other hand, all individuals showed an increase the seed output at 25°C, but those from northern localities increased more. T. officinale from all origins was not significantly affected by herbivory while native showed a negative effect. On the other hand, T. officinale exerted a strong negative effect on the native species, but this former not effected significantly to the invasive T. officinale. High plasticity and local adaptation in all ecophysiological traits, seed-set and the low cytogenetic variability in T. officinale suggests that both 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. officinale could perform successfully in environments with different climatic 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 given that a number of alien invasive plant species are colonizing broad geographical areas, several studies have focused on the strategies that enable their spread (Schweitzer and Larson 1999, 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 differentiation are 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, Sexton et al. 2002, Parker et al. 2003, Richards et al. 2006, Geng et al. 2007, Matesanz et al. 2010, Pichancourt and van Klinken 2012). Phenotypic plasticity and ecotypic differ-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, Joshi et al. 2001, Santamaría et al. 2003, Molina-Montenegro et al. 2010, Molina-Montenegro and Naya 2012). Plasticity may initially allow introduced species to become natural-ized across a range of environments (Sexton et al. 2002, Palacio-López and Gianoli 2011) and then heritable phenotypes may respond to local selection pressures, thus forming ecotypes better adjusted to local conditions (Sexton et al. 2002).

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

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

© 2012 The Authors. Ecography © 2012 Nordic Society Oikos Subject 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 and reproduction (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 (Strauss and Agrawal 1999) and may play a role in facilitating a successful invasion (Murren et al. 2005, Stastny et al. 2005). Physiological performance and herbivory, through their effects on plant fitness, may play a significant role in habitat colonization along environmental gradients.

It has been suggested that exotic species gain a competi-tive edge over natives because of their ability to exploit resources unavailable (or less available) to natives (Mack et al. 2000). A recent meta-analysis concluded that wide-spread alien plants are better able to capitalize on increased resource availability (Dawson et al. 2012). Changes in biomass in both natives and exotics have been used as a proxy to test their reciprocal competitive effects (Maron and Marler 2008). Phenotypic plasticity in morphological and/or physiological traits may grant plant success via increased resource capture, which would be reflected in changes 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, Gianoli and González-Teuber 2005, Baythavong and Stanton 2010, Molina-Montenegro et al. 2010), plants from populations located at higher latitudes are expected to show greater plasticity. Alternatively, plastic responses in plants at higher latitudes could not be of greater magnitude if costs of

plasticity, which constrain its expression (van Kleunen and Fischer 2005, Valladares et al. 2007), are more significant in stressful environments.

Taraxacum officinale (dandelion) is a worldwide distrib-uted species native to Europe (Fig. 1). It is considered one of the most aggressive invasive plants around the world (Holm et al. 1997). Taraxacum officinale is found growing in disturbed and undisturbed sites in wide altitu-dinal and latitudinal gradients (Molina-Montenegro and Cavieres 2010, Molina-Montenegro and Naya 2012). In South America it has a long latitudinal distributional range, from Colombia (12°N) to Tierra del Fuego in Chile (54°S), spanning hot-wet and dry-cold habitats (Molina-Montenegro and Naya 2012). It grows from sea level to 3600 m in the Andes of central Chile. Despite its remarkable distribution range and aggressive weed status, little is known about the physiological mechanisms that enable T. officinale to be successful in such a wide variety of habitats. In the present study we address phenotypic plasticity and ecotypic differentiation as possible explana-tions for the broad distributional range of T. officinale. We studied morphological, physiological, reproductive and cytogenetic traits in individuals of T. officinale grown from seeds collected in five localities along its latitudinal distribution range in South America. Specifically, we evalu-ated the occurrence of plastic and ecotypic responses in gas exchange traits, chlorophyll fluorescence, freeze toler-ance, and shoot morphology in plants exposed to two tem-peratures. Additionally, we evaluated seed production and ploidy level in plants growing at temperatures similar to those found at the extremes of the distribution gradient of T. officinale in South America. We also performed two manipulative experiments in order to assess whether the negative effects of simulated herbivory and inter-specific competition was greater in T. officinale than in a closely related native species.

Figure 1. Taraxacum officinale 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 officinale were collected in five localities: Manta (Ecuador), Trujillo (Perú), and La Serena, Valdivia and Punta Arenas (Chile). This latitudinal gradient covers from ca 0° to ca 54°S, including a significant thermic gradi-ent (Fig. 2, Table 1). All seeds were collected at sea level, to reduce altitudinal effects (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 of seeds. As T. officinale has apomictic reproduction (VaŠut 2003), samples were taken from widely separated plants to avoid 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 before sorting them into experimental treatments. Seeds from all localities were germinated in a room at 24 2°C on wet filter paper in Petri dishes and planted in 300-ml plastic pots filled with potting soil. First generation plants (F1) were generated from this initial seed pool and were grown in a

Figure 2. Geographic location of the populations of Taraxacum officinale used in the study. The elevation, latitude and longitude of each locality where the seeds were collected are shown.

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greenhouse at Univ. de Concepción, Concepción (36°48′S, 73°03′W) under natural conditions of light and temperature (1300 mmol m22 s21 50 and 22 2°C, respectively). These 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 achenes that were used to obtain experimental plants (F2).

Seedlings from all localities were planted in 300-ml plastic pots filled with potting soil. One week after the appearance of the first true leaf, seedlings were transferred to growth chambers (Forma Scientific) with a photon flux density (PFD) of 170 mmol m22 s21 and 16/8 h light/dark photoperiod. The two temperature treatments consisted of transferring 40 individuals from each locality described above to a growth chamber set at either 5°C or 25°C for 90 d. These temperatures were chosen because they are close to the mean temperatures in each extreme of the latitu-dinal gradient (Table 1). Plants at 5°C and 25°C 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 l21 once every 15 d. Plastic pots positions were randomized within the experimental plot every 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 between individuals from different populations.

Physiological performance

After 90 d of temperature acclimation, ten individuals from each locality at 25°C and another ten at 5°C were taken for fluorescence measurements at room temperature. Fluorescence signals (Maxwell and Johnson 2000) were generated by a pulse-amplitude modulated fluorometer (FMS 2, Hansatech, Instruments, Norfolfk, UK). One fully-developed attached leaf from each individual was dark-adapted for 30 min (to obtain open PSII centers) using leaf-clips to ensure maximum photochemical effi-ciency. The optic fiber and its adaptor were fixed to a ring located over the clip at approximately 10 mm from the sample and the different light pulses were applied (see below). Signal recordings and calculations were performed using the data analysis and control software provided with the instrument. Minimal fluorescence (F0) with all PSII reactions in the open state was determined by applying a weak modulated light (0.4 mmol m22 s21). Maximum fluorescence (Fm) with all PSII reaction centers in the closed state was induced by a 0.8 s saturating pulse of white light (9000 mmol m22 s21). After 15 s, the actinic

light (180 mmol m22 s21) was turned on and the same satu-rating pulse described previously was applied every 60 s until steady-state photosynthesis was reached, in order to obtain Fs and Fm′. Finally, F0′ was measured after turning off the actinic light and applying a 2 s far red light pulse (Pérez-Torres et al. 2004).

The same ten individuals used for fluorescence were selected 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 inserted into the Parkinson leaf cuvette of the IRGA, where net pho-tosynthesis and stomatal conductance were registered. All measurements were performed at midday, with photosyn-thetic active radiation (PAR) intensity provided by instru-ment (1200 mmol m22 s21) and at room temperature (20 2°C).

Thermal analysis

One expanded leaf with the apex removed was selected in seven different individuals from each population and each temperature treatment. Each leaf was attached to a thermocouple (Copper-constantan, Gauge 30; Cole Palmer Instruments, Vernon Hills, IL, USA) and immediately enclosed in a small, tightly closed cryotube to avoid changes in tissue water content. Temperature was continuously monitored and recorded (1 measurement per s) with an ACjr data acquisition board connected to a multi-channel tem-perature terminal panel (Strawberry Tree, Sunnyvale, CA, USA). The tubes were placed in a cryostat and the tem-perature was lowered from 0 to 215°C at a rate of approxi-mately 2°C h21. The temperature at the initiation of the freezing exotherm corresponds to the ice nucleation tem-perature, while the highest point of the exotherm represents the freezing temperature of the water in the apoplast (including symplastic water driven outwards by the water potential differences caused by apoplastic ice formation) (Larcher 1995, Bravo et al. 2001).

Shoot measurements

After the acclimation treatment, ten individuals from each locality were selected and the following traits were measured: leaf width and length (mm) and leaf dry biomass (mg, mean of three oldest fully-expanded leaves of each individual from each locality oven-dried for 72 h at 70°C). 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 were obtained 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. officinale from all sites and 20 individuals of H. scorzonerae. Two-months-old damaged plants suffered 25% defoliation with scissors (50% of leaf area removed in half the leaves; leaves were clipped along the mid-vein). We selected this kind of damage because it is commonly found in the field for these species (Molina-Montenegro unpubl.). Half the plants were subjected to artificial 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. The 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. whether performance patterns of Taraxacum officinale along a broad latitudinal gradient reflect either phenotypic plasticity or ecotypic differentiation, a two-way ANOVA was applied. Main factors were origin and temperature, and ecophysio-logical traits were the response variables. When factors were significant, differences in the mean of each ecophysio-logical trait were evaluated between populations with a Tukey test. Phenotypic plasticity will be inferred if the tempera-ture factor is significant, and ecotypic differentiation will be proved if the origin turns to be a significant factor. A sig-nificant interaction of factors will imply the occurrence of population differentiation in plasticity. Likewise, values of seed output per capitulum were averaged for each T. officinale individual, and this value was compared by two-way ANOVA between T. officinale individuals growing at 5 and 25°C and from each origin. Inspection of these fitness results will improve the interpretation of the first results (plasticity vs differentiation).

Similarly, we compared by two-way ANOVA the com-petition experiment and the effects of simulated herbivory. Comparisons between native and invasive species were con-ducted separately for each temperature because the aim of this study was to compare the competitive strength of the native and the invasive species growing under two temperatures rather than to evaluate the effect of tempera-ture on native-invasive relationships. For all ANOVAs, the assumptions of normality and homogeneity of variances were tested using the Shapiro–Wilks and Bartlett tests, respectively (Zar 1999).

Results

Physiological performance

Maximum photosynthetic efficiency (Fv/Fm) increased with temperature in all localities (Fig. 3A). The origin factor was also significant (Table 2). The Tukey test showed that Manta and Trujillo form a group with lower Fv/Fm than a second group conformed by La Serena, Valdivia and Punta Arenas (Fig. 3A). Additionally, the analysis did not show significant differences within these groups (Table 3). The interaction between origin and temperature was significant (Table 2). Although the maximum photosynthetic efficiency

Seed output

To assess the effects of temperature on seed output, F2 seedlings from each origin were chosen and transferred to walking growth chambers (Forma Scientific) with a photon flux density (PFD) of 200 mmol m22 s21 and 16/8 h light/dark photoperiod set at 5°C or 25°C for 100 d and irrigated daily and supplemented with Phostrogen (Solaris, NPK, 14:10:27) using 0.2 g l21 once every 15 d.

When capitula were closed indicating that seed development had begun, they were bagged with nylon-mesh bags to prevent seed loss. Bagged capitula were collected and seed output was calculated as the ratio between the number of fully filled seeds and the total number of seeds (i.e. inclu ding aborted and predated seeds) produced per capitulum.

Cytogenetic analysis

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

Interspecific competition and tolerance of herbivory

We evaluated competition between the exotic Taraxacum officinale from different origins along the latitudinal gradient and the native Hypochaeris scorzonerae, both members of the Asteraceae tribe Lactuceae. Both species co-occur along a 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, showy yellow heads and its seeds are mainly dispersed by wind (Matthei 1995). Seeds of H. scorzonerae (four to five per individual plant) were collected from a relatively large number of sampled plants (60–65) in La Serena and were germinated in a room with filter paper in Petri dishes as described above for T. officinale.

We calculated the relative competition intensity index (RCI; Grace 1995) between T. officinale (To) and H. scorzonerae (Hs) under two temperatures (5°C and 25°C) inside of growth chambers (same conditions as described above). To assess the competitive effect, 20 individuals of each species – and origin for T. officinale – were grown alone (mono culture) and 10 individuals of each origin of T. officinale were grown with 10 individuals of H. scorzonerae (one pair per pot of 500-ml 10 pots per situation) at two experimental temperatures. We focused on the outcome of competition between the invasive and the native species using final biomass (Bsp) as response variable. Thus, we assessed the competitive impact of Taraxacum from differ-ent origins on the native species (RCIHs [BHs Mono-culture 2 BHs Taraxacum]/BHs Monoculture), and the resistance of the native species to invasion by assessing its impact on Taraxacum (RCITo [BTo Monoculture 2 BTo Hypochaeris]/BTo Monoculture).

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Arenas increased even more (Table 3; Fig. 3B). Similarly to the net photosynthesis rate, stomatal conductance also increased significantly with temperature (Table 2); also, stomatal conductance was different between localities (Table 2). The interaction factor between temperature and origin proved to be significant, because although in all localities 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), net photosynthesis rate (Pn), stomatal conductance (g), ice nucleation temperature (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 at 5 or 25°C.

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 Taraxacum officinale 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 25°C. Significant differences between localities are denoted with different letters.

5°C 25°C

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 in Taraxacum officinale 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 at 5 and 25°C are shown.

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

Net photosynthesis rate was significantly higher at 25°C than at 5°C in all localities (Table 2). The analysis showed significant differences in the net photosynthesis rate among different localities, demonstrating again the presence of two groups (Table 3; Fig. 3B). The interaction factor between temperature and localities also was significant. Although all localities increased their net photosynthesis rates with temperature, La Serena, Valdivia and Punta

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Thermal analysis

Overall, the temperature at which apoplastic ice is formed was lower in individuals exposed to 5 than to 25°C (Table 2). Ice nucleation temperature changed significantly in individuals according to their origin (Fig. 4). Additionally, a posteriori test showed that Valdivia was the locality with the lowest ice nucleation temperature after 30 d of acclimation to 25°C, differing significantly from Punta Arenas and Manta (Table 3; Fig. 4). The interaction factor between origin and temperature was significantly different, because only Manta increased its ice nucleation point notoriously after 30 d of acclimation to 5°C (Fig. 4). On the other hand, Trujillo showed a lower nucleation tempera-ture after 30 d at 25°C than at 5°C, producing a crossed reaction norm (Fig. 4).

Shoot measurements

The width of leaves was significantly greater in plants kept at 25°C than at 5°C (Table 2; Fig. 5A). Overall, only the Trujillo locality differed significantly from other localities (Table 3). Additionally, the interaction effect was significant, because nearly all localities showed an increase in the width of leaves, with the exception of Punta Arenas, causing a crossed reaction norm (Fig. 5A). Similarly, the length of leaves was significantly greater at 25°C than at 5°C (Table 2). Additionally, the length of leaves differed among localities (Table 2; Fig. 5B). The interaction factor was also significant because the samples from Punta Arenas, La Serena, Trujillo and Manta showed a slight increase with temperature (Fig. 5B). The Valdivia population did not show any difference, causing a cross in the reaction norm (Fig. 5B). Dry mass increased significantly with temperature (Table 2), and was also different among localities (Table 2). The interaction factor showed significant differences, since the Trujillo locality increased its dry weight proportionally

Figure 5. Leaf width (A), leaf length (B), and total biomass (C) in Taraxacum officinale individuals after 90 d of acclimation at 5 and 25°C of temperature, from Manta (MA), Trujillo (TR), La Serena (LA), Valdivia (VA) and Punta Arenas (PA). Mean values ( 2 SE) at are shown.

Figure 4. Ice nucleation temperature (°C) in Taraxacum officinale individuals acclimated by 90 d at 5 and 25°C of temperature, from Manta (MA), Trujillo (TR), La Serena (LA), Valdivia (VA) and Punta Arenas (PA). Mean values ( 2 SE) at are shown.

more than Valdivia, La Serena and Manta while the Punta Arenas population did not show variation in dry mass with temperature (Table 3; Fig. 5C).

Seed output

Production of viable seeds in T. officinale growing at 25°C was 10% greater than in those individuals growing at 5°C

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

Competition and tolerance of herbivory

Taraxacum officinale from all sites showed higher success than native species. The relative competition intensity index (RCI) showed that T. officinale from all latitudes exerted strong competitive effects on H. scorzonerae, depressing its biomass from 65 to 34% at 25°C and from 48 to 33% at 5°C (Fig. 8). In contrast, native plants showed a weak effect on T. officinale, which showed from 36 to11% increase in biomass at 25°C and a increase in biomass from 21 to 14% at 5°C (Fig. 8). Additionally, T. officinale from northern localities (Manta and Trujillo) had greater negative effects on biomass of the native species, being this effect higher at 25°C than at 5°C (F4, 90 57.76, p 0.001 and F1, 90 107.16, p 0.001, respectively, Fig. 8). On the other hand, those individuals of T. officinale from southern localities (Valdivia and Pta. Arenas) grown with H. scorzonerae individuals significantly increased their bio-mass more than those from northern sites at 5°C, while at 25°C those T. officinale individuals from northern locali-ties (Manta and Trulillo) produced significantly higher biomass than those from southern populations (Fig. 8).

Overall, simulated herbivory decreased significantly the 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 5°C and 25°C (Fig. 9). Nevertheless, only for native species the treatment of simu-lated herbivory affected negatively and significantly these responses, being this decrease of 66 and 67% for Fv/Fm and a decrease of 77 and 65% for flower production at 5°C and 25°C, respectively (Fig. 9).

(Fig. 6); this difference was statistically significant (F1, 110 1430.21, p 0.001). Individuals from southern origins showed 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 effect was significant (F4, 110 71.1, p 0.001); although individuals from all origins showed high values of seed output at 25°C, those from Manta and Trujillo decreased more at low temperature (Fig. 6).

Cytogenetic analysis

The chromosome number in all Taraxacum officinale individuals from five localities was 24, revealing the ploidy

Figure 6. Seed output in Taraxacum officinale individuals accli-mated for 90 d at 5 and 25°C, 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 officinale 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 m.

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latitudinal gradient. Moreover, our analysis also detected differentiation in plastic responses. Changes in both physi-ology and morphology observed in T. officinale were mainly correlated to enhance their performance in the environ-ments similar to the origin. These results suggest that ecotypic differentiation and phenotypic plasticity are not mutually exclusive mechanisms for the successful establishment of T. officinale along the latitudinal gradient (Joshi et al. 2001). Several studies have shown that greater mor phological plasticity and ecotypic differentiation in response 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 and Griffin 2004).

Photochemical efficiency of photosystem II (Fv/Fm) in T. officinale individuals from all localities was greater at the higher temperature of acclimation. This suggests that the performance of photosystem II shows a plastic response. Similarly, in leaves of Secale cereale (winter rye), which natu-rally grows at ca 25°C, Fv/Fm decreased nearly 15% when they were cold acclimated at 5°C (Boese and Huner 1990). It has been suggested that plasticity in some traits that improve the Fv/Fm responses could help explain the spread in an invasive Mediterranean plant species (Traveset et al. 2008). On the other hand, net photosynthesis and stomatal conductance decreased substantially after cold acclimation in all the localities sampled. These results suggest an inhibition of photosynthetic capacity in plants after cold acclimation (Holaday et al. 1992, Brüggemann et al. 1994, Hurry et al. 1995). Gas exchange measurements in T. officinale revealed both plastic and ecotypic responses. Nagel and Griffin (2004), working with the invasive species Lythrum salicaria, showed that this plant species assimilated 208% 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 influence its invasive success. On the other hand, Horton et al. (2010) reported that the invasive species Miscanthus sinensis shows a rapid induction in photosynthetic parameters along a luminic gradient, indicating that a high photosyn-thetic rate allows greater carbon gain than native plants. Our results suggest that T. officinale is capable to adjust its physiological performance in such a way that resources are used efficiently in different abiotic conditions along the latitudinal gradient of distribution.

In the thermal analyses, only the locality of Manta decreased the temperature at which apoplastic ice is formed in tissue after cold acclimation, suggesting increased freeze resistance. In the other localities ice nucleation temperature was not affected by cold acclimation. Moreover, only indi-viduals from the Manta population showed an increment in the capacity to tolerate apoplastic ice formation after cold acclimation. This is a somewhat surprising result, con-sidering that Manta plants originally developed in a tropical climate. Cold stress is a selective factor that acts over longtime-scales and hence it may be assumed that localities in cold environments have undergone genetic differen-tiation rather than plasticity, allowing them to adapt their functioning to local conditions (Körner 2003). Nevertheless, we cannot rule out the possibility that the cold tolerance

Figure 8. Manipulative competition experiment between the native Hypochaeris scorzonerae (empty bars) and individuals of the invasive Taraxacum officinale (black bars) from all origins. Shown is the change in the biomass of the native and invasive species growing in monoculture and together in both at 5 and 25°C treat-ments. Mean values SD are shown. Different letters indicate significant differences; Tukey test, a 0.05.

Discussion

It has been suggested that reproductive traits as high seed output, high germination rate and apomictic reproduction will favor the establishment success of alien species (Heywood 1989, Pyšek 1997, Mullin 1998). Although high reproductive success reflects an enhanced physiologi-cal functioning in a given environment, the physiological mechanisms associated with a high performance in alien plants 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 geographical gradients have addressed the mechanistic basis of their success, and very few have determined whether they are adapted by plastic or ecotypic responses (or both) in func-tional and fitness-related traits.

Overall, our results show both phenotypic plasticity and ecotypic differentiation for all ecophysiological traits and fitness in T. officinale populations from the studied

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Figure 9. Simulated herbivory experiment in the native Hypochaeris scorzonerae and individuals of the invasive Taraxacum officinale from all origins. Shown is the physiological performance (Fv/Fm) and mean of flower production per individual of the native and invasive species with a 25% of fresh biomass cut at 5 and 25°C treatments. Mean values SD are shown. Asterisk indicate significant differences; ANOVA test, a 0.05.

observed in T. officinale from different localities could have evolved firstly in its home range (e.g. Alps, Molina-Montenegro et al. 2011).

Overall, a decrease in growth at 5°C was observed in T. officinale. This has been observed in other plant species: foliar area and dry weight decreased significantly during the first 30 d at 5°C in comparison with plants that were grown at 16°C (Boese and Huner 1990). Nevertheless, individuals from Punta Arenas did not show any significant difference in morphology when growing under contrasting temperatures. Lesser shoot growth was evident in plants from the two warmer localities (Manta and Trujillo) com-pared to those from colder environments (Valdivia and Pta. Arenas). Low temperatures retard cellular growth or dupli-cation in plants from alpine environments (Körner 2003). Thus, all individuals could have shown a decreased leaf growth by changes in the cellular function, being more evi-dent in those from warmer localities. On the other hand, those individuals from La Serena (intermediate latitude and tem-perature) showed the highest biomass accumulation, sug-gesting the influence of a factor other than temperature. Considering that La Serena has the driest environment of all the study sites, and that low temperature induces a water stress for cells (Nobel 2005), higher biomass in those individuals from La Serena could reflect, at least in part, a tolerance response to water shortage rather than temperature effects.

Based on our results we suggest that T. officinale is capable of invading a broad latitudinal gradient by a combination of phenotypic plasticity and genetic differentiation, as has been shown for other invasive plant species (Sexton et al. 2002, Parker et al. 2003, Maron et al. 2004). Several studies have indicated that plasticity may entail a cost for plants (DeWitt et al. 1998, van Kleunen and Fischer 2005, Valladares et al. 2007, Auld et al. 2010). It is thus likely that the plasticity showed by T. officinale as a strategy to cope with environmental pressures along of the latitudinal gradient may have involved a cost. Such a putative ‘cost of plasticity’ should be clearly observed in fitness-related traits. However, all individuals showed a similar seed production and physiological performance at 25°C and the mean value of these traits was greater in those populations with higher plasticity. Therefore, plasticity costs were not detected for T. officinale in this study.

The triploid condition of T. officinale individuals from all localities studied agrees with a positive correlation between polyploidy and invasiveness (Pandit et al. 2011, Beest et al. 2012) and suggests that they are apomictic. This condition is generally associated with a low genetic variability (Allen and Otto 1994). Nevertheless, unexpectedly high levels of genetic variation have been found in others apomictic spe-cies populations, suggesting the occurrence of genetic segre-gation in the apomicts generated by subsexual reproduction

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plasticity and ecotypic differentiation in ecophysiological traits are one of the main mechanisms that allow this species to spread along wide environmental gradients.

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

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