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Functional differences in response to drought in the invasive Taraxacum officinale from native and introduced alpine habitat ranges

Marco A. Molina-Montenegroa; Constanza L. Quirozb; Cristian Torres-Díazc; Cristian Atalad a Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile b Laboratorio de Invasiones Biológicas, Universidad de Concepción, Concepción, Chile c Laboratio de Genómica & Biodiversidad (LGB), Departamento de Ciencias Naturales, Universidad del Bío-Bío, Chillán, Chile d Departamento de Ciencia y Tecnología Vegetal, Universidad de Concepción, Campus Los Ángeles, Chile Accepted uncorrected manuscript posted online: 07 April 2011 Online publication date: 10 June 2011 To cite this Article Molina-Montenegro, Marco A. , Quiroz, Constanza L. , Torres-Díaz, Cristian and Atala, Cristian(2011)

'Functional differences in response to drought in the invasive Taraxacum officinale from native and introduced alpine habitat ranges', Plant Ecology & Diversity, 4: 1, 37 — 44, doi: 10.1080/17550874.2011.577459, First posted on: 07 April 2011 (iFirst) To link to this Article: DOI: 10.1080/17550874.2011.577459 URL: http://dx.doi.org/10.1080/17550874.2011.577459

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Plant Ecology & Diversity Vol. 4, No. 1, March 2011, 37–44

Functional differences in response to drought in the invasive Taraxacum officinale from native and introduced alpine habitat ranges Marco A. Molina-Montenegroa *, Constanza L. Quirozb , Cristian Torres-Díazc and Cristian Atalad

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a Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile; b Laboratorio de Invasiones Biológicas, Universidad de Concepción, Concepción, Chile; c Laboratio de Genómica & Biodiversidad (LGB), Departamento de Ciencias Naturales, Universidad del Bío-Bío, Chillán, Chile; d Departamento de Ciencia y Tecnología Vegetal, Universidad de Concepción, Campus Los Ángeles, Chile

Background: Phenotypic plasticity and ecotypic differentiation have been suggested as the main mechanisms by which widely distributed species can colonise broad geographic areas with variable and stressful conditions. Some invasive plant species are among the most widely distributed plants worldwide. Plasticity and local adaptation could be the mechanisms for colonising new areas. Aims: We addressed if Taraxacum officinale from native (Alps) and introduced (Andes) stock responded similarly to drought treatment, in terms of photosynthesis, foliar angle, and flowering time. We also evaluated if ontogeny affected fitness and physiological responses to drought. Methods: We carried out two common garden experiments with both seedlings and adults (F2) of T. officinale from its native and introduced ranges in order to evaluate their plasticity and ecotypic differentiation under a drought treatment. Results: Our data suggest that the functional response of T. officinale individuals from the introduced range to drought is the result of local adaptation rather than plasticity. In addition, the individuals from the native distribution range were more sensitive to drought than those from the introduced distribution ranges at both seedling and adult stages. Conclusions: These results suggest that local adaptation may be a possible mechanism underlying the successful invasion of T. officinale in high mountain environments of the Andes. Keywords: ecophysiological traits; high-mountain environments; invasive species; local adaptation; plasticity; Taraxacum officinale

Introduction Water shortage usually induces several morphological changes (Grace 1997; Pedrol et al. 2000), decreases in the photosynthetic rate (Flexas et al. 2006; Galmés et al. 2006) and reduces flowering time (Rajakaruna et al. 2003; Heschel and Riginos 2005; Sherrard and Maherali 2006). In plants subjected to drought, the maximum quantum yield (Fv/Fm) and photochemical efficiency (PS II) drop below optimal values (Posch and Bennett 2009). Thus, fluorescence measurements are a good estimator of the physiological functioning of plants (Maxwell and Johnson 2000). Drought also affects leaf angle (King 1997) and root:shoot ratio (Quiroz et al. 2009). Drought-exposed plants usually have their leaves at a more acute angle to reduce the incident radiation and invest more resources to below-ground structures to maximise water uptake. Plant species have developed mechanisms to cope with stressful environments. Phenotypic plasticity and ecotypic differentiation have been suggested as the main mechanisms through which widely distributed plant species can colonise broad geographic areas with variable and stressful conditions (Sexton et al. 2002). Phenotypic plasticity and ecotypic differentiation are two complementary strategies to face environmental heterogeneity (Platenkamp 1990; *Corresponding author. Email: [email protected] ISSN 1755-0874 print/ISSN 1755-1668 online © 2011 Botanical Society of Scotland and Taylor & Francis DOI: 10.1080/17550874.2011.577459 http://www.informaworld.com

Counts 1992; Sexton et al. 2002; Maron et al. 2004). It has been shown that plasticity can initially allow exotic species to become naturalised in their non-native range (Sexton et al. 2002). Once naturalised, genetic recombination of heritable phenotypes may respond to local selection pressures, giving rise to ecotypes with higher fitness (Ellstrand and Schierenbeck 2000). In fact, both plasticity and ecotypic differentiation can contribute to broaden the distribution and abundance of plant species across an environmentally heterogeneous landscape (Galen et al. 1991; Joshi et al. 2001; Santamaría et al. 2003; Geng et al. 2007). Plant development is generally accompanied by major changes in morphology and physiology. These ontogenetic changes represent the unfolding of a developmental programme where phenotypic plasticity can affect the timing of such changes (Diggle 2002). In many cases, developmental stage and environment alter the functional relationship between traits, as measured by shifts in allometric slope or intercept (Weiner 2004). As a consequence, conclusions regarding phenotypic plasticity may dramatically differ if ontogenetic changes in phenotypic expression are taken in consideration (Valladares et al. 2006). Invasive species are among the most widely spread plant species (Rejmánek et al. 1989). Many alien invasive

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species successfully colonise broad geographical areas, thus, several studies have focused on the mechanism that enable them to spread (Geng et al. 2007). Most of the studies on the invasion process have focused on traits related to reproduction, survival, and competitiveness (e.g. Chun et al. 2007), but less attention has been paid to physiological traits (but see Richards et al. 2006). In an array of different environments, reproductive success and competitiveness of invasive plants will firstly depend on adequate physiological functioning. However, examples of physiological mechanisms that provide an advantage for invasive species in different environments are infrequent in the literature (e.g. Williams et al. 1995; Nagel and Griffin 2004; Eggemeyer et al. 2006; Molina-Montenegro et al. 2010). In addition, the potential effects of ontogenetic changes on plasticity and their indirect effects on biological invasions have received little attention (Fumanal et al. 2007; Valladares et al. 2007). Taraxacum officinale Weber ex. F.H. Wigg. (Asteraceae) is an invasive plant that was introduced in Chile as a weed from Europe ca. 150 years ago (Matthei 1995; Holm et al. 1997). Within high elevations of the Alps (which is part of it native range) T. officinale is mostly restricted to disturbed sites with a mesic growing season. Similarly, in the Andean zone of central Chile (introduced range) this exotic species is abundant either in disturbed sites or undisturbed natural communities (Cavieres et al. 2005). However, in contrast to the Alps, the Andes of central Chile are under the influence of the Mediterranean-type climate that occurs in lowlands. This climate is characterised by a very dry growing season (Table 1), during which plants suffer severe drought stress (Cavieres et al. 2005). T. officinale is mainly apomictic, which means it reproduces through unfertilised ovules that are genetically identical to the mother plant (van Dijk 2003). In the present study we assessed the effect of drought on the ecophysiological responses of T. officinale from the Alps (native range) and the Andes (introduced range) through a common garden experiment. In addition, we evaluated if developmental stage affected the response to drought in both native and introduced T. officinale individuals. Since maternal effects have been shown to affect some ecophysiological traits in many invasive species, in this study we used the F2 generation of both populations to avoid such effects. Table 1. Summary of climatic conditions at the French Alps (45◦ N) and at the Andes of central Chile (33◦ S). Climatic records were obtained for a range of altitude (2600–2900 m a.s.l.) from WorldClim over a period of time of 30 years. Variable

Alps

Andes

Mean annual precipitation (mm) Mean precipitation of warmer quarter (mm) Precipitation seasonality (CV) Mean annual temperature (◦ C) Mean temperature of warmer quarter (◦ C)

1560 336 11.2 1.0 8.5

503 20 92.0 5.6 10.7

Materials and methods Bulk collections of T. officinale seeds were made in the Queyras Mountains, south-western French Alps at 2600 m a.s.l. (native range) and in the Molina River valley, central Chilean Andes at 2700 m a.s.l. (introduced range). Due to the influence of the Mediterranean-type climate, drought conditions in the Andes of central Chile are more accentuated than in the majority of the mountains in the Alps (Cavieres et al. 2006). A few achenes per individual (3–4) were collected from a relatively large number of maternal plants (over 100) per site. F1 plants were generated from this initial seed pool and were grown in a greenhouse at the Universidad de Concepción, Concepción under controlled conditions of light and temperature (1320 ± 55 µmol m−2 s−1 and 22 ± 2 ◦ C, mean ± S.E.). These plants were put in 300-ml plastic pots filled with organic potting soil and irrigated every 2 days with 100 ml of water. After ca. 5 months these plants produced the achenes that were used to obtain experimental plants (F2). Subsequently, achenes were germinated at 24 ± 2 ◦ C on wet filter paper in Petri dishes and planted in 300 ml plastic pots filled with potting soil and randomly assigned to the different treatments explained below.

Drought effects To compare the response of T. officinale to drought, 7 days after the appearance of the first true leaf, 40 seedlings from both origins were planted into 1-litre plastic pots (one plant per pot) filled with a 1:1 mixture of commercial soil and sand. After 7 days, seedlings were randomly assigned to two treatments: (1) addition of 100 ml of water every 2 days (watered) and (2) addition of 100 ml of water every 5 days (drought). The drought treatment in the plastic pots inside of the glass-house at the Universidad de Concepción mimicked the soil matric potentials that are found in both south-western French Alps and the Andes of central Chile during the driest period of the growing season, respectively (Quiroz et al. 2009, Table 1). After 3 months, 13 individuals from each population and from each treatment were randomly selected for fluorescence measurements at room temperature. Fluorescence signals were generated by a pulse-amplitude modulated fluorometer (FMS 2, Hansatech, Instruments Ltd, Norfolk, UK). Leaves were dark-adapted using leaf-clips to ensure maximum photochemical efficiency. We considered maximum quantum yield of PS II (Fv/Fm; where Fv = [Fm – F0 ], Fm, maximum fluorescence yield; and F0 , minimum fluorescence yield) as the photosynthetic performance parameters (Maxwell and Johnson 2000). In the same way, we recorded the photochemical efficiency (PS II) and electron transport rate (ETR) as parameters of physiological efficiency for comparison under drought vs. control conditions (Maxwell and Johnson 2000). In addition, after 3 months, we measured the foliar angle and root:shoot ratio in 12 individuals each from the Alps

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and the Andes to search for mechanisms of drought tolerance. Changes in foliar angle have been interpreted as a mechanism to dissipate heat and to avoid photoinhibition (Molina-Montenegro and Cavieres 2010). Root:shoot ratio is expected to increase with drought. Finally, the number of heads produced was recorded every 3 days in all individuals.

Ontogenetic effects To compare the response to drought of seedlings and adults of T. officinale from both origins, a manipulative experiment was made. Seven days after the appearance of the first true leaf, 30 seedlings from each origin were planted into 1-litre plastic pots filled with 1:1 mixture of commercial soil and sand. In order to evaluate the effect of drought on seedlings, 7-day-old seedlings were assigned to two treatments: (1) addition of 100 ml of water every 2 days (watered) and (2) addition of 100 ml of water every 5 days (drought). Similarly, to evaluate the effect of drought on adults, 4-month old individuals were assigned to two treatments: (1) addition of 100 ml of water every 2 days (watered) and (2) addition of 100 ml of water every 5 days (drought). Before the beginning of the experimental treatments, all individuals were irrigated with 100 ml of water every 2 days. Experiments made with seedlings and adults were conducted separately. After 6 months, 15 individuals from each origin and from each treatment were randomly selected for fluorescence measurements, as described above. In addition, survival was recorded weekly until physiological measurements were made.

Statistical analysis The effects of drought treatment on fluorescence variables (Fv/Fm, PSII and ETR), foliar angle and root:shoot ratio were compared using two-way ANOVAs. For all two-way ANOVAs, the assumptions of normality and homogeneity of variances were tested using the ShapiroWilks and Bartlett tests, respectively (Zar 1999). The effect of ontogeny (seedlings vs. adults) on maximum photochemical efficiency (Fv/Fm) was analysed with a Kolmogorov–Smirnov two-sample test. To compare the survival curves of seedlings and adults of T. officinale individuals with early and late drought were estimated by means of the Kaplan-Meier method, and statistical differences were assessed with the Cox-Mantel test (Fox 1993).

Results Drought effects Maximum photosynthetic efficiency (Fv/Fm) decreased with water shortage in both origins but not in the same fashion (interaction, F48,1 = 173.64; P < 0.001; Figure 1A). The individuals from the Alps showed a greater decrease

Figure 1. (A) Maximum quantum yield (Fv/Fm), (B) photochemical efficiency of PSII (PS II) and (C) electron transport rate (ETR) of photosystem II in Taraxacum officinale individuals from the Andes (filled circles) and the Alps (open circles). Mean values (± 2 SE) in fluorescence parameters after 3 months of watered (+H2 O) and drought (–H2 O) treatments are shown. (Different letters indicate significant differences; Tukey test, α < 0.05).

(Figure 1A). Although PS II significantly decreased with water shortage in plants from both origins (Figure 1B), the interaction between factors (F48,1 = 35.53; P < 0.001) indicated that the decrease was higher in Alpine individuals than in Andean plants. ETR significantly decreased with water shortage in the Alpine (Figure 1C) but not in the Andean individuals (interaction, F48,1 = 298.12; P < 0.0001). Root:shoot ratio was significantly enhanced (F44,1 = 73.52; P < 0.001) in the drought treatment

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Figure 3. Flowering percentage along time in Taraxacum officinale individuals from the Andes and the Alps under watered (+H2 O) and drought (–H2 O) treatments.

Figure 2. Foliar angle (A) and root-shoot ratio (B) in Taraxacum officinale individuals from the Andes (filled circles) and the Alps (open circles). Mean values (± 2 SE) are shown. (Different letters indicate significant differences; Tukey test, α < 0.05).

(Figure 2A). Additionally, the interaction effect (origin x water availability) was significant (F44,1 = 21.95; P < 0.0001). Although plants from both origins increased the root:shoot ratio with drought, individuals from the Alps showed a higher increase (Figure 2A). Leaf angles were significantly enhanced (F44,1 = 525.70; P < 0.001) by drought (Figure 2B). Similarly, the interaction effect (origin x water availability) was significant (F44,1 = 364.79; P < 0.001). Although plants from both origins increased the foliar angle with respect to ground level under drought, individuals from the Alps showed a higher increase (Figure 2B). The percentage of flowering of individuals from both origins was higher in the watering treatment than under drought (Figure 3). Maximum flowering percentage was reached by watered individuals from the Andes with 83%, followed by watered plants from the Alps and plants from the Andes under drought with 75% and 67%, respectively. Individuals from the Alps under drought did not produce flowers (Figure 3). Ontogenetic effects The maximum PPS II of T. officinale seedlings from the Alps decreased significantly earlier than in plants from the Andes (0 week, P = 0.95; 4 weeks, P = 0.011; 8 weeks,

P = 0.003; 12 weeks, P = 0.021), showing evidence of photoinhibition before the first month (Figure 4A). In the same way, adults from the Alps showed a significantly earlier decrease in maximum photochemical efficiency (0 week, P = 0.87; 4 weeks, P = 0.84; 8 weeks, P = 0.078; 12 weeks, P = 0.046; 16 weeks, P = 0.011; 20 weeks, P = 0.008), compared to conspecifics from the Andes (Figure 4B). In the seedling and adult stages, the survival of T. officinale individuals from the Andes was significantly higher than in those from the Alps (value of Cox–Mantel test = 15.1, P = 0.002). A sharp decrease in survival was observed in seedlings from the Alps during the first month. Moreover, all individuals died within 16 weeks (Figure 5A). In contrast, seedlings from the Andes showed less mortality with ca. 50% of seedlings alive at end of the experiment (Figure 5A). Adults of T. officinale from both origins showed a similar decrease in survival under watered conditions. Alpine individuals showed a sharp decrease in survival as soon as the drought treatment was applied (Figure 5B, Cox–Mantel test = 4.2, P = 0.029). No individuals from the Alps were alive at the end of the experiment, while Andean individuals maintained ca. 50% survival (Figure 5B). Discussion Our results suggest local adaptation in T. officinale for all ecophysiological traits assessed. The changes observed in T. officinale populations from the Alps and Andes were consistent with the environmental characteristics of the growing season in each place of origin. This result suggests ecotypic differentiation as a likely mechanism for the successful establishment of T. officinale in its non-native environment, in accordance with previous propositions for establishment in contrasting and stressful environments (Geng et al. 2007; Molina-Montenegro and Cavieres 2010). The performance of photosystem II (PS II and Fv/Fm) was higher in watered compared to drought treatment for

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Local adaptation in the invasive Taraxacum officinale

Figure 4. Maximum photochemical efficiency (Fv/Fm) along time in seedlings (A) and adults (B) of Taraxacum officinale from the Andes and the Alps under watered (+H2 O; filled circle) and drought (–H2 O; open circle) treatments. Mean values (± 2 SE) are shown. Broken line indicates the start of drought treatment.

both origins. Lower PS II and Fv/Fm in the droughtexposed plants are related to a lower photosynthetic rate and therefore, to greater photoinhibition. This is a common plant response to drought (Maxwell and Johnson 2000; Gallé et al. 2007; Posch and Bennett 2009). Similarly, electron transport rate (ETR) was higher under watered conditions. Moreover, only individuals from the Alps showed a decrease in ETR when exposed to drought, suggesting that individuals from the Andes can tolerate water shortage conditions by maintaining robust physiological functioning and efficient mechanisms of energy dissipation. Overall, both high photochemical efficiency and ETR under drought in Andean individuals suggest that mild water limitation is not a major stress factor for them in the field. Thus, T. officinale from the Andes may be adapted to the ‘new condition’ of drought by using alternative pathways for electrons transport, such as photorespiration, which may help avoid photoinhibition (Franco and Lüttge 2002). The higher invasive potential of the individuals from the Andes may be related to these properties. Accordingly, in a previous study, Quiroz et al. (2009) showed that T. officinale from the Alps was more sensitive to soil characteristics

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Figure 5. Survival in seedlings (A) and adults (B) of Taraxacum officinale from the Andes and the Alps under watered (+H2 O; filled circle) and drought (–H2 O; filled circle) treatments. Mean values (± 2 SE) are shown. Broken line indicates the start of drought treatment.

(e.g. water shortage) than conspecifics from the Andes, suggesting that the capacity to tolerate a dry growing season could be a key trait for a successful invasion in the Andes, and possibly other zones with Mediterranean-type climate. Foliar angle and root:shoot ratio were affected under drought only in the individuals from the Alps, where the growing season is more mesic than in the Andes (Table 1). Variations in the foliar angle have been previously documented as a strategy to avoid water loss through transpiration under drought and/or high irradiance (Patiño and Grace 2002), which allows plants to reduce their physiological activity (Ikeda and Matsuda 2002). In the same way, increases in root:shoot ratio have been documented as typical strategies to cope with water shortage in order to enhance the contact area for water uptake (Hunt and Nicholls 1986; Quiroz et al. 2009). Watered individuals from the Andes showed the highest flowering percentage, followed by individuals from the Alps in the watered treatment, then by individuals from the Andes under drought, and finally by those from the Alps under drought. Several studies have shown that flowering

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is a plastic response for many plant species (Fox 1990; Passioura 2006). In fact, an early flowering – similar to that observed in the Andes – has been shown to be selected in some environments, particularly under water-limiting conditions (Franks et al. 2007). Although, T. officinale from the Alps modified their foliar angles and root:shoot ratio as mechanisms to decrease the detrimental effects of drought in comparison with individuals from the Andes, these modifications did not affect flower production. Ontogeny did not affect the main trends in Fv/Fm and survival in response to drought. Both seedlings and adults from the Andes were less plastic than their counterpart from the Alps (Figure 4 and 5). This means that whatever differences in plasticity exist in T. officinale seedlings from native and invasive ranges in response to drought, they are maintained throughout the ontogeny. Some plant species exhibit different degrees of plasticity from seedlings to adults (Coleman et al. 1994; Valladares et al. 2006). Contrary to our findings, Mediavilla and Escudero (2004) found that plasticity to drought in physiological traits can vary from seedling to adults in Mediterranean oaks (Quercus spp.), mainly as a result of the variation in the capacity of their roots in accessing soil water and variation in their stomatal behaviour. Compared with our results, it suggests that ontogenetic effects in traits related to regulating water relations are stronger in woody species than in herbaceous ones. While plants from the native range (Alps) had more plasticity and suffered a higher fitness reduction in response to drought, plants from the invasive range (Andes) showed less plasticity and maintained a relatively constant fitness under the same conditions, as previously reported for other traits (Quiroz et al. 2009). These results suggest that local adaptation rather than plasticity could be the likely explanation for T. officinale being a successful invader in the Andes. It has been suggested that apomictic plants may be better colonisers of extreme environments, such as alpine environments, than sexually reproducing plants (Lynch 1984). It is possible that apomictic plant populations could differentiate into ecotypes more rapidly than strictly sexual populations. To our knowledge, no study has assessed the likelihood of ecotypic divergence in apomictic and sexual populations of T. officinale. On the other hand, T. officinale can be treated as different sub-species according the traits evaluated. Thus, the populations from the Alps used in this study are probably not the source population of the Andes populations. Hence, the ecotypic differentiation suggested in this study could be the result of pre-adaption at infra-specific level in the native range, followed by successful establishment in the Andes, rather than a local differentiation of the introduced Alps genotypes in the Andes. Further experiments with an appropriate sampling design are required to test this hypothesis. Finally, since the first record of this species in Chile is from the city of Santiago in 1870, multiple introductions have probably taken place since then (Matthei 1995).

Although our study area in the Andes is close to Santiago (50 km), it seems unlikely that this species has been present there for more than 100 years. The functional differentiation in some ecophysiological traits of T. officinale suggests that this invasive plant species can definitively adapt to local environmental conditions in their new habitats. Acknowledgements We thank Ernesto Gianoli and Fernando Valladares for their valuable comments on early versions of the manuscript. This research was supported by the MECESUP UCO 0214 project. This paper forms part of the research activities of the Center of Biotechnology for the Development in Arid Zones (BIOTECZA).

Notes on contributors Marco A. Molina-Montenegro is titular researcher at the Centro de Estudios Avanzados en Zonas Áridas (CEAZA), La Serena. His main lines of research are functional plant ecology in stressful environments and biological invasions mechanisms. Constanza L. Quiróz is a researcher in the Biological Invasions Laboratory at the Universidad de Concepción, Concepción. She studies the process of invasion in the mountain environments. Cristian Torres-Díaz is professor in Biology at the University of Bío-Bío, Chillán, Chile. He studies the ecology, biogeography, and conservation biology of Chilean flora. Cristian Atala is professor in Biology at the University of Concepción, Los Angeles. His main research lines are functional ecology of climbing plants, and the anatomical study of the structure-function relationships of vascular tissues.

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