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Physiology and Development |
2Division of Biological Science, University of Missouri, Columbia, Missouri 65211-0074 USA
Received for publication December 20, 2004. Accepted for publication May 25, 2005.
ABSTRACT
We compared water relations and adaptations to drought stress in native and invasive exotic dandelions, Taraxacum ceratophorum and T. officinale. Photosynthesis (A), transpiration (E), and water use efficiency (WUE; carbon gained/water lost) were measured for the two species under extreme drought in the alpine tundra of Colorado, USA. We also subjected both species and F1 hybrids to a dry-down experiment to determine how relative physiological performance varied with water availability. Photosynthesis and transpiration in the field were low and did not differ between Taraxacum congeners; however, native T. ceratophorum had higher WUE than T. officinale. After 6 days of greenhouse drought, photosynthesis and transpiration were reduced in T. officinale compared to T. ceratophorum. Taraxacum ceratophorum maintained high WUE under control and drought treatments. Conversely, WUE in T. officinale was highly plastic between watered (low WUE) and dry-down (high WUE) treatments. Hybrids did not exhibit heterosis; instead, they were similar to T. officinale in A and E and intermediate to the parental species in WUE. Overall, results suggest that native dandelions are more drought tolerant than invasive congeners or their hybrids, but have less plasticity in WUE. Arid habitats and occasional drought in mesic sites may provide native dandelions with refugia from negative interactions with invasives.
Key Words: drought tolerance • hybrid • invasive species • physiological performance • Taraxacum • water use efficiency
Although many factors including propagule pressure, competitive ability, biological characteristics of exotic species, and genetic diversity influence the likelihood of invasion by exotic species, recent theory suggests that the availability of under-utilized resources in a plant community correlates positively with invasibility (Davis et al., 2000
; Davis and Pelsor, 2001
). Increased resource availability either directly through input (e.g., increased precipitation) or indirectly through a reduction in resident species (e.g., disturbance) may facilitate establishment of exotic populations. As a result, extreme environments where productivity is commonly limited by resource availability may be less permeable to invasion than those with high resource availability (Stohlgren et al., 1999
, 2001
), providing refuge to native species more adapted to these harsh conditions. One such environment is the alpine tundra, in which native plant species experience strong selection from short growing seasons, low temperatures, drought, nutrient limitations, heavy winds, and high levels of solar radiation (Billings, 1987
; Kammer and Mohl, 2002
). Depending upon the incidence of these stress factors in space or time, exotic species may be less successful than natives at establishing viable populations in alpine habitats. However, all communities are invasible (Williamson, 1996
), and exotic species that are successful may more efficiently use or monopolize limiting resources than native plants (Tilman, 1985
, 1988
; Vitousek, 1986
). To address how functional traits influencing competitive ability vary between invasive exotic and noninvasive native species, we compare the water use efficiency and photosynthetic rates of closely related dandelions (Taraxacum) that occur in sympatry.
For plants, a high rate of net carbon assimilation (A) can result in higher biomass accumulation, favoring future growth and reproduction as well as competitive status (Aarssen and Clauss, 1992
; Arntz et al., 1998
, 2000
; Aarssen and Keogh, 2002
). However in C3 plants, collecting atmospheric CO2 necessitates the loss of water vapor (Kramer and Boyer, 1995
), and when water is limited, high photosynthetic rates should come at a cost (Arntz and Delph, 2001
). Instantaneous water use efficiency (WUE = A/E), the ratio of net carbon assimilation rate (A) over transpiration rate (E), is a measure of how a plant copes with this trade-off. Invasive plants often have higher rates of carbon assimilation and/or water use efficiency relative to native plant species, which may contribute to their spread (Pattison et al., 1998
; Baruch and Goldstein, 1999
; Durand and Goldstein, 2001
; McDowell, 2002
). Currently, many invasive—native comparisons are between distantly related species, which can be confounded by differences in taxonomic history (Harvey and Purvis, 1991
). Our study adds to a small but growing number of physiological comparisons between congeneric native and invasive species.
Interspecific hybridization represents another possible avenue through which exotic species could achieve competitive superiority over native congeners. Certain novel hybrid genotypes may have unique combinations of parental traits that confer competitive superiority (Arnold and Hodges, 1995
; Rieseberg and Carney, 1998
), and vigorous fertile hybrids may ultimately displace plants of parental species (Ellstrand, 1992
; Levin et al., 1996
; Wolf et al., 2001
). Studies of crop species suggest that additive gene action is often the major mode of inheritance for photosynthetic rate (Ellison et al., 1983
; Hobbs and Mahon, 1985
; Simon, 1994
) and water use efficiency (Percy et al., 1996
; Malik et al., 1999
). Additive inheritance should produce first-generation hybrid phenotypes intermediate to parentals for photosynthetic rates or WUE in hybrid offspring. Alternatively, if hybrids show heterosis in physiology, they may outperform exotic and native parental genotypes, due to a demographic advantage (e.g., increased plant vigor and fecundity). Ultimately, under this scenario, hybrid establishment could allow exotics to "mine the native gene pool" for selectively advantageous traits enabling future backcrosses to undergo local adaptation (Stebbins, 1942
; Anderson, 1949
; Lewontin and Birch, 1966
; Rieseberg and Wendel, 1993
). To address this idea, we compare the physiological performance of native and exotic Taraxacum species and their interspecific hybrids under contrasting levels of drought stress in the greenhouse.
Fossil evidence indicates that T. ceratophorum, the alpine dandelion, is native to North America, occurring at least 100 000 yr ago in Alaska (Chaney and Mason, 1936
; Richards, 1973
). In its current range, populations of T. ceratophorum co-occur with T. officinale, the common dandelion, which was introduced to North America during European settlement (Solbrig, 1971
; Scott, 1995
; Mack, 2003
). Although T. officinale sets seed asexually through diplosporous agamospermy (Asker and Jerling, 1992
), asymmetrical hybridization can result if pollen is transferred from T. officinale onto stigmas of the outcrossing T. ceratophorum (Brock, 2003
, 2004
). Taraxacum officinale and T. ceratophorum are sympatric in alpine Colorado (Rocky Mountains, USA; Brock, 2004
). This region is characterized by extreme monthly and yearly variation in rainfall (Peterson and Billings, 1982
; Galen et al., 1999
), and studies have shown that growth in resident plant species is commonly water limited (Johnson and Caldwell, 1975
; Peterson and Billings, 1982
; Enquist and Ebersole, 1994
). Furthermore, at our field site on Pennsylvania Mountain (Park County, Colorado, USA), soil moisture determines seedling establishment in sympatric Epilobium angustifolium (Onagraceae) and periods of drought result in mortality of established plants of Polemonium viscosum (Polemoniaceae) (Galen, 2000
; A. Dona and C. Galen, unpublished data).
In the summer of 2002, Colorado had a drought that was ranked the driest of 108 yr (May to August, National Climate Data Center, Colorado). We compared physiological performance and efficiency of T. ceratophorum and T. officinale plants during this drought period. The Taraxacum congeners and their interspecific hybrids were subsequently raised in the greenhouse and their physiological performance compared under high and low water availability. We asked the following questions: (1) Do native and exotic dandelion species differ in physiological responses to extreme drought in the field? (2) Do Taraxacum congeners differ in their physiological responses to drought or in traits affecting drought tolerance under a common environment (greenhouse)? (3) Do hybrids show heterosis for photosynthetic rate or water use efficiency? (4) Do parental species and/or hybrids differ in suites of traits related to carbon assimilation rate and/or to water use efficiency? (5) Is T. officinale physiologically superior to T. ceratophorum in either photosynthesis or water use efficiency?
MATERIALS AND METHODS
Study system
Taraxacum ceratophorum grows from the tree-line (krummholz, 3505 m a.s.l.) upwards into the open alpine tundra at our study site on Pennsylvania Mountain (Park County, Colorado, USA; 39°15' N, 106°07' W). Within this transition zone, T. officinale is sympatric with T. ceratophorum plants in open meadows and at the margins of willow (Salix glauca) stands. The T. ceratophorum population is composed of diploid plants (2n = 16), and intraspecific crosses confirm that plants have an obligately outcrossing breeding system (Brock, 2004
). Triploid T. officinale plants (3x = 24) are apomictic, producing fertile seed in the absence of pollination (King, 1993
; Holm et al., 1997
; Lyman and Ellstrand, 1998
). Both Taraxacum species produce a basal rosette of leaves anchored by a thick taproot. Although these congeners have similar inflorescences, T. ceratophorum plants have clasping, horned bracts (phyllaries) subtending the inflorescence, which can be used to discern them from T. officinale plants, which have hornless reflexed phyllaries. Flowering phenologies overlap from mid-June to August, and insect visitors move indiscriminately between inflorescences of the two species (Brock, 2003
). Moreover, hand-pollination of T. ceratophorum stigmas, using T. officinale plants as pollen donors, produces interspecific hybrids (Brock, 2003
, 2004
).
Physiological responses to extreme drought in the field
In June 2002, plants of T. ceratophorum and T. officinale were selected along 50-m transects in each of two habitat types; open meadows (open, N = 10 plants per species) and next to stands of the willow, Salix glauca (willow, N = 10 plants per species). On 3–4 July 2002, gas exchange measurements were conducted using a LI-COR 6400 infra-red gas analyzer (LI-COR, Lincoln, Nebraska, USA). Light intensity (Photosynthetically active radiation, PAR) within the sampling chamber was set at 2000 µmol · m–2 · s–1, using an LI-6400-02B LED light source (LI-COR). The CO2 flow into the chamber was maintained at a concentration of 350 µmol · mol–1, using a LI-6400-01 CO2 mixer (LI-COR). Temperature control targeted a leaf temperature of 20°C to maintain leaf temperature at the ambient level in the face of changing transpiration rates. We monitored instantaneous carbon assimilation rate (A; µmol CO2 · m–2 · s–1) and transpiration rate (E; mmol H2O · m–2 · s–1), and calculated water use efficiency (WUE = A/E, µmol CO2/mmol H2O). Measurements were taken on healthy leaves of comparable age in the rosette (one leaf per plant) in the morning (0900–1130 hours) and were alternated between the two species. Following physiological measurements, each leaf was removed, pressed, measured with a CID leaf area meter (Model 201; CID, Vancouver, Washington, USA) to correct gas exchange measurements for surface area, and stored for carbon isotope analysis. The following day (5 June), soil cores adjacent to each Taraxacum plant were removed, placed in individual sealed plastic bags, weighed (wet mass), dried in an oven to constant mass (48 h at 60°C), and reweighed (dry mass). Soil water content was estimated as (wet mass–dry mass)/dry mass (Brower et al., 1997
). Rainfall at the field site was monitored starting on 1 June and indicates that on the initial measurement day plants in both habitats had not received rainfall for at least 32 d.
The carbon isotope ratio of leaf tissue (
13C) indicates long-term WUE integrated over the lifetime of the leaf (Wright et al., 1988
; Farquhar et al., 1989
; Anderson et al., 1996
). Plants with lower long-term WUE have more negative 13C values. Using the stored leaf samples, we compared 13C of native and exotic plants in open and willow habitats, and although decreased irradiance levels can reduce 13C (Farquhar et al., 1989
), replicates of both species were sampled from the habitat neighboring willow stands. Dried leaves from all 40 plants were individually ground in liquid nitrogen, and samples were analyzed for the carbon isotope composition on a PDZ Europa Science 20-20 mass spectrometer (Center for Stable Isotope Biogeochemistry, University of California at Berkeley, California, USA). Analysis on one leaf failed, reducing the sample size for T. ceratophorum (N = 19).
Data analysis
Instantaneous measures of gas exchange (A, E, WUE) and soil water content were compared between species using analysis of variance (ANOVA, PROC GLM, Statistical Analysis System, version 6.12; SAS Institute, Cary, North Carolina, USA) with species, habitat, and the species x habitat interaction designated as fixed effects. To meet assumptions of ANOVA, photosynthetic rate (A), and water use efficiency (WUE) were square-root transformed, and transpiration rate (E) was log transformed. Residuals of the 13C values (
) were not normally distributed. Rank-transformed 13C data (nonparametric Friedman's test, PROC RANK, SAS) and nontransformed data were analyzed with an identical model as described earlier. Trends and conclusions did not differ between the two methods, and therefore we present the parametric analysis. The relationship between instantaneous WUE and 13C (rank-transformed) was tested for significance by Pearson's product-moment correlation (r).
Physiological responses to experimental drought and traits affecting drought tolerance in the greenhouse
To compare physiological responses of T. ceratophorum, T. officinale, and interspecific hybrids to varying moisture regimes in a common environment, we conducted a dry-down experiment in the greenhouse (University of Missouri, Columbia, Missouri, USA). In 2002, we collected seeds from 15 randomly sampled plants of each parental species in the open habitat on Pennsylvania Mountain. Seedlings from each open-pollinated T. ceratophorum plant likely represent a mixture of half- and full sibs, while those of each T. officinale plant are (barring somatic mutation) genetically identical. Hybrid seedlings were obtained by planting seeds from 15 interspecific crosses between randomly selected plants of each parental species. Crosses were conducted in the field (Pennsylvania Mountain) in 2001 (Brock, 2004
). For each cross, T. ceratophorum recipients were pollinated daily with a different randomly selected T. officinale pollen donor. Consequently, hybrid seedlings from each cross probably represent a mixture of half-sibs and full sibs. Hybrid genotype was verified for seedlings resulting from interspecific pollination using a species-specific microsatellite marker (Brock, 2004
).
Seeds were sown on 18 December 2002 in trays of peat growing medium (Pro-Mix BX Professional General Purpose Growing Medium; Premier Horticulture, Red Hill, Pennsylvania, USA). Due to low and uneven germination, species-specific sample sizes were reduced to the following maternal families containing four siblings or two siblings: T. ceratophorum (7 and 1, respectively), hybrid (8 and 5, respectively), and T. officinale (6 and 2, respectively). On 6 January 2003, seedlings were transplanted individually into 1.5-L pots containing Pro-Mix medium. Plants were distributed randomly in the greenhouse, fertilized with osmocote slow-release fertilizer (14-14-14 N-P-K, Osmocote, Scotts Company, Marysville, Ohio, USA), and watered every other day. On 3 February, each individual was transplanted into a 7.57-L pot containing a 3 : 1 mixture of Pro-Mix : fritted clay (Hi-Dri clay absorbent, Sud-Chemie Absorbents, Meigs, Georgia, USA). Fritted clay retains water, decreasing the rate of water loss under experimental drought and enabling plants to acclimate more naturally to dry conditions (T. Dawson, University of California, Berkeley, personal communication). The greenhouse temperature was regulated by air conditioners set to a high of 21°C, and although PAR varied over the course of the day, it peaked at 1482 ± 130 µmol · m–2 · s–1 under clear skies.
Plants from each maternal family were randomly assigned to either a watered treatment (control; 400 mL daily) or a drought treatment (no water for 6 d), yielding pairs (N = 15, 21, 14 for T. ceratophorum, hybrid, and T. officinale, respectively) of control and droughted siblings per species. Gas exchange measurements were conducted for both plants in each sibling pair in two trials, at the onset (initial) and end (final) of the dry-down experiment. Native, exotic, and hybrid sibling pairs were randomly (but evenly with respect to species sample size) scheduled for initial gas exchange measurements on one of four consecutive dates (cohorts, 17–20 March). For each cohort, final measurements were recorded on the sixth day of the dry-down treatment. Within each cohort, a sibling pair from each native, exotic, and hybrid group was randomly selected over time (1300–1600 hours), and within each pair the sequence of measurements was randomized.
Gas exchange rates (A and E) were made as before using a LI-COR 6400 except that CO2 concentration was raised to 370 µmol · mol–1 to match the ambient level in the greenhouse. In addition, soil water content (SWC) and leaf relative water content (RWC) were sampled for each plant to monitor the effectiveness of the dry-down treatment. Prior to each gas exchange measurement, a soil core was removed from each pot, sealed in a plastic bag, weighed (wet mass), dried in a drying oven (60°C for 48 h), and reweighed (dry mass). Soil water content was estimated as (wet mass–dry mass)/dry mass. We followed methods of Barrs and Weatherly (1962)
to measure leaf relative water content. A leaf disk (11 mm diameter) was removed (after gas exchange measurements to avoid any bias due to wounding) from a randomly selected healthy mature leaf on each plant and immediately weighed (fresh mass). Leaf disks were floated on distilled water (5°C) for 24 h prior to reweighing (saturated mass) and then dried for 48 h in a drying oven (60°C) to obtain a final dry mass measurement. Relative water content was calculated as (fresh mass–dry mass)/(saturated mass–dry mass). These leaf disk samples were also used to estimate specific leaf area (SLA; surface area/dry mass). A few samples were lost reducing final sample sizes by two for SWC (one T. ceratophorum plant and one hybrid plant) and two for RWC and SLA (two T. officinale plants).
Data analysis
Variation in instantaneous rates of gas exchange (A and E), WUE, SWC, RWC, and SLA was analyzed using separate split-plot mixed model ANOVAs (PROC GLM, SAS). Fixed effects in the model consisted of species, treatment, and trial (initial vs. final measurements) with date of measurement (cohort) included as a random effect (Steel et al., 1997
). To meet assumptions of ANOVA, E was square-root transformed and values of SWC, RWC, and WUE were rank transformed prior to the analysis (PROC RANK, SAS). Results from rank transformed and nontransformed data were compared; trends and conclusions did not differ for RWC and WUE parameters. We present results of the parametric tests for WUE and RWC and ranked results for SWC. Significant trial x species x treatment interactions were followed by separate mixed model ANOVAs for each trial, followed by post-hoc Tukey's tests.
We used planned contrasts of plants in each treatment group (final trial) to test if hybrid plants were more vigorous than parental species. Hybridization between triploid (apomict) and diploid (sexual) Taraxacum species commonly produces triploid apomictic offspring (Richards, 1970
; Morita et al., 1990
; Tas and van Dijk, 1999
). Ovules in sexual Taraxacum species are haploid, and formation of triploid offspring indicates unbalanced genetic contributions of parental species (2 apomict : 1 sexual). We used the following planned contrast weightings (2 : 1) to control for differences in genetic contributions of T. officinale and T. ceratophorum, respectively, when testing for hybrid vigor in A and WUE.
To test whether species vary in combinations of traits that influence rates of resource capture or the efficiency of resource capture, we conducted a principal components analysis (PROC FACTOR, options CORR and VARIMAX; SAS) on final measurements of A, E, WUE, RWC, and SLA, transformed as before to meet assumptions of parametric analysis. The first two axes (eigenvalues > 1) were subjected to mixed model ANOVA (PROC GLM, SAS) with species and treatment as fixed factors and cohort as a random effect.
RESULTS
Physiological responses to extreme drought in the field
Percentage soil water content did not vary significantly between microsites containing the two species, with habitat, or with the species x habitat interaction (Table 1, P > 0.23 for all tests). Average SWC (5.14 ± 0.88% [here and elsewhere, ± 95% confidence limits]) reflected extreme drought during this period. Rates of photosynthesis (A) and transpiration (E) in the field did not vary between species or with habitat (Table 1, P > 0.41 for all tests; Fig. 1). Habitat differences and the species x habitat interaction were also not significant for instantaneous WUE (Table 1, P > 0.23 for all tests). However, plants of T. ceratophorum were 40.9% more water-use efficient than plants of T. officinale (F1,36 = 10.94, P < 0.0021; Fig. 1). As expected, instantaneous WUE was correlated with long-term water use efficiency as indexed by 13C (r = 0.48, P < 0.002). The average 13C for T. ceratophorum differed significantly from that of T. officinale (–26.00 ± 0.36 and – 27.38 ± 0.35, respectively; F1,35 = 31.35, P < 0.0001). This pattern is consistent with greater integrated WUE for native dandelions relative to exotics. In the field, native plants are less wasteful of water under drought over instantaneous and long-term time scales and appear to be better adapted to dry alpine conditions. Delta 13C values also varied with habitat (F1,35 = 8.74, P < 0.0055). Plants neighboring willows had lower 13C values (less water-use efficient) than plants in open meadows (– 27.05 ± 0.35 and – 26.33 ± 0.36, respectively). However the species x habitat interaction was not significant (F1,35 = 1.58, P > 0.217).
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Specific leaf area did not vary significantly between treatments, trials, or their interaction (P > 0.11 for all tests, Table 2). However, species varied significantly in SLA. On average, SLA was similar for T. officinale and hybrid plants (279.8 ± 26.3 cm2/g and 282.9 ± 20.3 cm2/g, respectively; Tukey's test, P > 0.9727) and significantly greater than SLA of T. ceratophorum (236.0 ± 24.2 cm2/g, both Tukey's tests, P < 0.0542).
The PCA identified two major components (eigenvalues > 1), together accounting for 76% of the variation for the five traits measured (Table 4A). The first principal component (PC1) explained 52% of the variance and was positively correlated with A, E, and RWC. The second component (PC2) explained an additional 24% of the variance and was positively correlated with WUE and negatively correlated with SLA. This pattern suggests that variation in traits related to carbon assimilation rate was independent of variation in traits influencing water use efficiency. After drought, variation among species in PC1 scores differed between treatments (species x treatment interaction, F2,9 = 9.84, P < 0.0054). Under control conditions, species did not vary significantly in PC1 scores (Tukey's test, P > 0.70 for all comparisons). Under drought, native dandelions had significantly higher values for a combination of traits related to carbon gain (PC1) than either exotics or their hybrid. Mean PC1 scores of T. officinale and hybrids were similar (Tukey's test, P > 0.7210) and significantly lower than the mean PC1 score of T. ceratophorum (Tukey's test, P < 0.0011 for all comparisons; Fig. 4). This result shows that native dandelions have higher values for a combination of traits related to carbon gain under drought than either exotics or their hybrid. Differences among species represent the only significant source of variation in PC2 scores in the experiment (F2,6 = 10.03, P < 0.0122, Table 4B). Plants of T. officinale did not differ significantly from hybrids in mean PC2 score (Tukey's test, P > 0.855) and, on average, both had significantly lower scores on PC2 than plants of T. ceratophorum (Tukey's test, P < 0.0192 for both; Fig. 4).
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Under extreme drought, natural populations of T. ceratophorum and T. officinale showed no significant difference in photosynthetic rate. Rates observed in the field were very low relative to maxima under benign (control) conditions in the greenhouse. In the greenhouse, photosynthetic rates of Taraxacum species were similar under control conditions, but diverged in response to drought. After experimental drought photosynthesis dropped in T. officinale, but was unaffected in T. ceratophorum. Overall, our results suggest that drought tolerance in T. ceratophorum confers physiological advantages under moderate water stress, but not under rare episodes of prolonged stress. Instantaneous and integrated measures of water use efficiency were significantly higher in T. ceratophorum than T. officinale in the field and (for instantaneous WUE) in the greenhouse. Adaptation to drought in T. ceratophorum is indicated by the production of thicker leaves (low SLA) and maintenance of higher WUE compared to T. officinale or hybrids. Hybrids did not show heterosis in physiological traits, but were intermediate to parental phenotypes in WUE and more like T. officinale in A and E.
We measured physiological performance of native and invasive Taraxacum species across a wide range of water availability. In 2002, natural populations on Pennsylvania Mountain experienced the most severe drought in 108 yr and had not received rain for at least 32 d prior to measurement. At the other end of the spectrum, plants in greenhouse control conditions were watered daily. The greenhouse drought treatment represents an intermediate level of water stress (6 d of drought). In the central Rocky Mountains, an average of 
5 d passes between rainfall events during the summer months (June–August, 17 yr of data recorded at Hoosier Pass, 8 km northeast of Pennsylvania Mountain; University of Nevada, Western Regional Climate Center, http://www.wrcc.dri.edu). Although soil type influences soil moisture available to plants (Brady, 1984
), differences in soil water content among field drought (5.14%), greenhouse drought (61.2%), and greenhouse control (147%) also show that our study qualitatively encompassed a broad continuum of water availability for these Taraxacum plants. Because gas exchange measurements were taken under nearly identical leaf chamber conditions in the greenhouse and field, it is possible to view the environments as points along a continuum of drought stress, recognizing that other sources of variation (plant age, phenology, etc.) may also have influenced plant performance.
Under extreme drought and well-watered conditions, T. ceratophorum and T. officinale did not differ significantly in mean photosynthetic rate on a per unit area basis. However after moderate greenhouse drought, T. ceratophorum plants maintained mean carbon assimilation at control levels, while T. officinale plants experienced severe reductions (Fig. 3). The similarity in mean photosynthetic rates for greenhouse droughted and naturally droughted T. officinale plants (respectively, A = 5.3 ± 2.5 µmol CO2 · m–2 · s–1 and 5.7 ± 2.8 µmol CO2 · m–2 · s–1) indicates that T. officinale is intolerant of moderate and severe drought. Additionally, RWC of T. officinale dropped from 90% in control conditions to 59% under drought in the greenhouse. Reduced A of T. officinale may reflect failure to maintain leaf RWC under drought (Fig. 2). Conversely, plants of T. ceratophorum maintained high leaf RWC (90%) across greenhouse treatments. C3 plants with RWC from 75 to 90% commonly decrease stomatal conductance to regulate plant water status, reducing carbon assimilation due to limitations in internal CO2 (Lawlor and Cornic, 2002
). At progressively lower RWC (below 75% RWC), metabolic limitation (e.g., water limitation of ATP synthesis, Rubisco molecules, electron transport) further reduces carbon assimilation (Tezara et al., 1999
; Lawlor and Cornic, 2002
).
Under drought stress, plants with higher WUE should be able to accumulate more biomass than less water-use efficient plants, providing a selective advantage for increased WUE (Donovan and Ehleringer, 1994
; Dudley, 1996
; Heschel et al., 2002
). Instantaneous and long-term WUE in the natural population were positively correlated and indicate that, in comparison with T. officinale, T. ceratophorum should fix more carbon per unit of water lost. Although plants bordering willows had lower long-term water use efficiency (more negative 13C values) than those in the open, the change in habitat affected long-term WUE of Taraxacum congeners equivalently. High WUE was maintained for T. ceratophorum plants across greenhouse and natural conditions (Figs. 1 and 3). Conversely, T. officinale was more variable in WUE. In the greenhouse, T. officinale control plants had lower WUE than those of T. ceratophorum, but exhibited a plastic increase in WUE in response to experimental drought. Taraxacum officinale plants likely increase instantaneous WUE by reducing stomatal conductance in response to drought stress. Gas and water exchange at the leaf surface are typically correlated, and analysis (not shown) indicates that, under drought stress, stomatal conductance in T. officinale falls with transpiration rate.
Measurements of WUE in T. officinale plants under drought in the greenhouse and in nature differ, suggesting that WUE may decline with increasing severity of drought. Alternatively, increased CO2 partial pressure in the greenhouse relative to the higher altitude alpine site may help account for the unique capacity of the greenhouse T. officinale to increase carbon assimilation per unit water lost (Bowes, 1993
). Taken together, field and greenhouse results suggest that T. ceratophorum is more canalized for high WUE and for tolerance of frequent water limitation. Conversely, T. officinale plants exhibit greater plasticity, maximizing photosynthesis under mesic conditions, while increasing water regulation during periods of moderate drought stress.
The drought tolerance and high WUE of T. ceratophorum should favor growth in water-limited habitats and/or under episodic drought. Furthermore, T. ceratophorum maintained rates of carbon assimilation equal to or higher than those of T. officinale plants across a wide range of soil moisture, suggesting that drought tolerance and high WUE in T. ceratophorum is not a liability to resource capture on a per area basis. However, further field experiments are needed to predict the outcome of interspecific competition between T. ceratophorum and T. officinale under water limitation.
Plants adapted to alpine conditions have a suite of morphological adaptations that can reduce water demands: small leaves, reduced leaf surface area, and lower shoot to root ratios (Billings and Mooney, 1968
; Körner et al., 1989
; Körner, 1999
). Plants of T. ceratophorum exhibit at least two of these adaptations: reduced aboveground surface area (Brock, 2003
; Brock et al., 2005
) and small SLA (16% less than T. officinale). These finding suggests that populations of T. ceratophorum have become locally adapted to the dry growing seasons of the central Rocky Mountains, in contrast to sympatric populations of T. officinale. Our results conflict with previous findings of higher photosynthetic rate (Pattison et al., 1998
; Baruch and Goldstein, 1999
; Durand and Goldstein, 2001
) and WUE (McDowell, 2002
) for invasive species than for co-occurring natives. The discrepancy between our findings and studies of other invasive plants suggests that the physiological basis of competitive status may vary widely among invasive plant taxa and/or among invaded habitats.
Physiological performance of interspecific hybrids
Hybrids between T. ceratophorum and T. officinale did not physiologically outperform either parental species. Instead, hybrids resembled the paternal T. officinale parent in physiology under control and drought conditions, suggesting maternal inheritance plays a minor role in accounting for variation in photosynthetic rates. Hybrids were intermediate to, and not significantly different from, mean WUE of the two parental species under well-watered conditions and did not demonstrate plasticity for increased WUE under drought stress. Based on planned comparisons of parental genetic contributions in Taraxacum, mean hybrid phenotypes are not significantly different from the predicted parental intermediate phenotype for A under control or drought conditions. Similarly, hybrid mean WUE is also intermediate to the parental phenotypes. Additive gene action appears to account for variation in both traits under control and drought conditions, supporting previous findings for A (Ellison et al., 1983
; Murthy et al., 1991
; Malik et al., 1999
) and WUE (Schuster et al., 1992
; Gorny, 1999
; Malik et al., 1999
).
Although hybrids do not on average outperform parental species, vigorous hybrid offspring with unique combinations of parental ecophysiological traits could still proliferate. Selection acts on individuals and should favor fit hybrid offspring from the possible range of parental trait combinations (Arnold and Hodges, 1995
). After drought, the maximum rate of carbon assimilation measured in hybrid plants was 65% greater than the mean for T. ceratophorum. Although gene flow from parental species often swamps out hybrid genotypes in sexual species (Levin, 1975
; Arnold, 1997
), hybrid offspring of apomictic and sexual Taraxacum parents are commonly apomictic themselves (Morita et al., 1990
; Tas and van Dijk, 1999
). Furthermore, hybrid plants are capable of asexual seed production while potentially siring backcross progeny. If the variation among hybrids in physiological performance under drought has a genetic basis, selection on rare but fit apomictic hybrid lineages could result in the proliferation of vigorous hybrid ecotypes.
Patterns of character correlation
Physiological and morphological traits cluster into two composite variables, which explain 76% of the total phenotypic variation. Because principal components are orthogonal, the analysis suggests that traits affecting resource assimilation rate (PC1) are independent of traits affecting water use efficiency (PC2) across the contrasting conditions used in our experiment. The pattern of variation in PC1 reinforces univariate analyses in showing superior drought tolerance of native dandelions. Variation between species in PC2 provides a mechanism for native superiority. Leaves of T. ceratophorum are thicker (lower SLA) and more water-use efficient than those of T. officinale. Plants in arid environments generally have lower SLA, which correlates with higher water use efficiency (Cunningham et al., 1999
; Westoby et al., 2002
; Reich et al., 2003
). Thick leaves are common in alpine plants and often result from an increase in palisade cell layers and in intercellular air space (Körner et al., 1989
; Atkin et al., 1996
; Körner, 1999
). Due to the higher concentration of photosynthetic proteins per area, thicker leaves should more efficiently assimilate internal CO2 while limiting stomatal conductance (Reich et al., 2003
). Although potential limitations in leaf nitrogen concentration can constrain the enhanced CO2 assimilation in thicker leaves, alpine plants often have higher concentrations of leaf nitrogen content than those at lower altitudes (Körner et al., 1986
). Our results indicate that native and invasive Taraxacum species differ in suites of physiological and morphological traits that may influence persistence under drought. Native T. ceratophorum plants exhibit adaptations favored in environments where water limitation is frequent in space (e.g., xeric microsites) and/or time (e.g., periods of drought). Drought may help to limit invasion by T. officinale and drought-prone sites may provide refugia for native T. ceratophorum.
Conclusion
Results of this study indicate that physiological superiority of native and invasive Taraxacum depends on abiotic environmental conditions. In the absence of water limitation, plants should maximize carbon assimilation by opening stomata (Cohen, 1970
; Heschel et al., 2002
). Taraxacum officinale plants have greater aboveground surface area (Brock, 2003
; Brock et al., 2005
) coupled with a greater capacity to extract water from the soil. These advantages may confer growth advantages for exotic dandelions in mesic environments. However, as water becomes limiting, species differences in characters influencing drought tolerance (SLA, WUE, and small size) should favor T. ceratophorum plants, yielding a competitive advantage for natives under drought (Tilman, 1988
). According to this idea, continued intermittent periods of drought should help slow invasion of high alpine ecosystems by T. officinale. However, other possible changes in environmental conditions, including an increase in atmospheric CO2, could alleviate the severity of water limitation to photosynthesis in the alpine and favor the continued spread of T. officinale.
FOOTNOTES
1 The authors thank two anonymous reviewers, J. Birchler, K. Cone, T. Holtsford, and D. Larsen for their helpful comments on this manuscript; A. Dona and M. Carter for assistance in the field; S. Pallardy for advice on the greenhouse experiment; M. Ellersieck for aid in the statistical analysis; B. Sonderman for continual care of greenhouse plants; T. Holtsford for access to laboratory equipment; and the University of Colorado for access to field sites on Pennsylvania Mountain. This research was funded by a TWA Scholarship (2002–2003) to M. Brock and NSF grant DEB 0087412 to C. Galen. 
3 Author for correspondence (e-mail: brockmt{at}umn.edu
) present address: Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 USA; phone: 612-624-3124, fax: 612-625-1738
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