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Ecology |
Oregon State University, 321 Richardson Hall, Environmental Science Program, Corvallis, Oregon 97331 USA
Received for publication January 22, 2002. Accepted for publication April 25, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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13C). Using discriminant analysis, these photosynthetic characteristics were found to be powerful in distinguishing between the invasive and noninvasive Rubus. Amax and A/E were identified as the most useful variables for distinguishing between the species, and therefore, may be important factors contributing to the success of these invasive species.
Key Words: photosynthetic capacity • photosynthetic nitrogen-use efficiency • specific leaf area • water-use efficiency
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; D'Antonio and Vitousek, 1992
; Hobbs and Mooney, 1998
; Mack et al., 2000
). In spite of the serious impacts of invasive plants, the mechanisms that confer their vigor are not adequately explained by current theories and hypotheses (Bazzaz, 1986
; Mack, 1996
). The magnitude of the threats imposed by invasive plants has motivated much research on invasions, particularly on predicting additional invasions and developing control methods. However, we still lack a fundamental understanding of the mechanisms by which invasive plants succeed, an understanding that may eventually improve predictive and control capabilities (Baruch and Goldstein, 1999
; Mack et al., 2000
).
Several characteristics common to invasive plants have been identified to facilitate recognition and prediction of future invaders, such as high reproductive allocation, rapid vegetative growth rates, and high potential for acclimation (Bazzaz, 1986
; Rejmanek, 1996
). Physiological characteristics of invasive plants have also been identified by contrasting invasive species with unrelated noninvasive species (Pattison, Goldstein, and Ares, 1998
; Baruch and Goldstein, 1999
). An effective approach to identify mechanisms of invasive plant success is through the comparison of closely related invasive and noninvasive congeners that overlap in range and share morphological and life-history traits (Schierenbeck and Marshall, 1993
; Mack, 1996
). The advantage of comparing congeners rather than unrelated species is that it provides more insight into which traits actually play a role in the invasiveness of a species and which are merely coincidental (Mack, 1996
). The mechanisms that underlie the success of the invasive species may be found among those characteristics that distinguish them from similar species that are not considered invasive.
One mechanism by which invasive plants may achieve success is through maximizing photosynthesis (Baruch and Goldstein, 1999
; Durand and Goldstein, 2001
). High photosynthetic rates may be obtained by maximizing the biochemical capacity for photosynthesis. The biochemical capacity to photosynthesize can be assessed by relating net photosynthesis (A) to varying internal leaf CO2 concentrations (Ci), also known as A/Ci curves (Wullschleger, 1993
). The components of photosynthetic capacity that may be determined from A/Ci curves include the carboxylation capacity (Vcmax), which is constrained by the amount and activity of the enzyme ribulose 1, 5-bisphosphate carboxylase-oxygenase (Rubisco), and the chloroplast electron transport capacity (Jmax), which is constrained by the amount of thylakoid membranes.
Photosynthesis can be limited by low nitrogen or water availability. Therefore, maximizing A relative to nitrogen and water costs may be another mechanism of invasive plant success. Both Rubisco and thylakoid-bound electron transport carriers represent a major investment in leaf nitrogen (N), so there is typically a positive relationship between photosynthetic capacity and leaf N. The ratio of A to leaf N, or photosynthetic nitrogen-use efficiency (PNUE), is an indicator of resource capture per unit investment (Field and Mooney, 1986
). Additionally, a high rate of photosynthesis per unit water loss (water-use efficiency, WUE) is a mechanism by which invasive plants may increase the efficiency of resource capture. The ratio between rates of A and transpiration (E) provides an instantaneous measure of WUE. Measurements of integrated WUE are obtained from the relative abundance of the stable isotopes of 13C and 12C in plant tissue (13C). During photosynthesis, plants discriminate against 13C due to a combination of diffusional and enzymatic processes. Increases in A/E reduce the concentration of CO2 within the leaf due to increased consumption of CO2 relative to the supply, thereby forcing photosynthesis to consume relatively more 13C and resulting in increased 13C of plant tissue. The positive relationship between A/E and 13C is well established for many species (Farquhar, O'Leary, and Berry, 1982
; Johnson et al., 1990
; Knight, Livingston, and Van Kessel, 1994
).
An additional possible mechanism contributing to invasive plant success is the minimization of carbon costs associated with photosynthesis, leaving more carbon available for growth and reproduction. For example, leaf area per unit leaf mass (specific leaf area, SLA) is an indicator of photosynthetic surface area per unit investment in leaf tissue and is often positively associated with rapid growth rates (Lambers and Poorter, 1992
; Reich, Ellsworth, and Walters, 1998
; Walck, Baskin, and Baskin, 1999
). In one comparative study between invasive and noninvasive congeners in which both species had similar photosynthetic rates, the greater success of the invasive species was partly attributed to its thinner leaves, and therefore, lower carbon cost per unit photosynthetic area (Pammenter, Drennan, and Smith, 1986
). Lower carbon costs of leaf construction (CC) (Baruch and Goldstein, 1999
; Nagel and Griffin, 2001
) and higher A relative to dark respiration rates (Rd) (Pattison, Goldstein, and Ares, 1998
) have also been found for invasive species in comparison with noninvasive species from other genera. One study also observed a negative correlation between species abundance and leaf CC for one invasive and several noninvasive species growing together along pond banks (Nagel and Griffin, 2001
).
The objective of this research was to compare physiological characteristics of four similar noninvasive and invasive Rubus (blackberry) species, two of which are prolific and vigorously invasive species. All of the species share similar morphologies and life history, and they often occupy the same sites in the Pacific Northwest of the United States (PNW), but the two invasive species have strikingly greater rates of growth and reproduction. Given the similarities among the Rubus species in the PNW, the differences among their growth and reproductive rates become even more remarkable. The physiological mechanisms that underlie these differences may play a role in the success and vigor of these invasive species. This study focuses on instantaneous measurements of photosynthesis and resource costs. An additional, simultaneous study examines how these rates and costs translate into annual carbon gain, reproductive effort, and growth (McDowell and Turner, in press). The following hypotheses were tested: (1) invasive Rubus species have higher photosynthetic capacity than similar noninvasive species, and (2) invasive Rubus species achieve these rates at a lower resource investment than the noninvasive species. The rate and efficiency at which these invasive species acquire carbon may contribute to their vigor, and thus invasiveness, in the PNW.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and produce over 700 fruits in a single year (McDowell and Turner, in press). Rubus laciniatus Willd. (lace-leaf blackberry), also an invasive species, is similar in size and fruit production to R. discolor, but may be distinguished by its highly dissected leaves. These two species contrast with the noninvasive R. ursinus Cham. and Schlect. (trailing blackberry) and R. leucodermis Dougl. (black raspberry). These species are considered noninvasive in their native range in the PNW where this study took place. Canes of these species grow to merely 2 m and produce only about 50–100 fruits per cane per year (McDowell and Turner, in press). Aside from differences of size and reproductive allocation, these species share similar morphologies. All have perennial roots with arching and sprawling biennial canes (i.e., canes reproduce only in the second year). First-year canes emerge in the spring. Foliage is maintained on these canes until the following spring, when second-year foliage emerges, except for R. leucodermis, which sheds first-year foliage in the fall. All second-year foliage and canes senesce after reproduction is completed in the second growing season. These species often inhabit the same sites throughout the PNW, growing in open areas and forests at predominantly low elevations.
Gas exchange was measured on all four species growing together at three sites within 10 km of each other in the McDonald-Dunn Research Forest near Corvallis, Oregon (44°40' N, 123°20' W; 210–360 m elevation). Measurements were made on one fully exposed leaf per cane and all leaves of all species were of similar age and position on the canes. Vapor pressure deficit (vpd) concurrent with these measurements was calculated using humidity and temperature data from a nearby (<5 km) meteorological station. The diurnal patterns of instantaneous WUE of each species were examined with respect to diurnal patterns of vpd. Additionally, five leaves of R. discolor and R. ursinus were collected from each of three other sites in western Oregon to assess how foliar 13C varies for these species across a wider range of sites. These sites included Jack Creek (43°41' N, 123°24' W; 207 m elevation), Alsea Fish Hatchery (44°24' N, 123°45' W; 69 m elevation), and Kiser Creek (44°29' N, 123°30' W; 500 m elevation) and cover a range of approximately 100 km.
Gas exchange measurements
Rates of A in relation to varying internal leaf CO2 concentrations (A/Ci curves) were measured in the field with an LI-6400 infrared gas-exchange system (LI-COR, Lincoln, Nebraska, USA). Measurements were made on 6–9 leaves per species per month during spring and summer (April–August) and less frequently during fall and winter (September–March). All measurements were made before 1000 on overcast days to minimize effects of increasing ambient vpd and temperature. The order of species measured was random. During all measurements, temperature was 23° ± 4°C and vpd was 1.1 ± 0.3 kPa inside the cuvette. Photon flux density within the cuvette was held at approximately 1500 µmol·m–2·s–1. Enough time was allowed for the cuvette [CO2] to stabilize before logging measurements (i.e., coefficient of variation for [CO2] inside the cuvette <2%). Three measurements per leaf were made at each of the following cuvette [CO2]'s: 10, 20, 30, 40, 60, 80, 100, and 150 Pa.
The A/Ci curves for each species were used to calculate biochemical photosynthetic capacity and Rd. Parameters of photosynthetic capacity include the maximum carboxylation rate (Vcmax), maximum electron transport rate (Jmax), and the maximum rate of net photosynthesis measured under saturating light, optimal ambient temperature and humidity, and ambient CO2 concentration of 36.5 Pa (Amax). Light saturation levels for each species were determined by measuring A in relation to varying levels of radiation for each species (data not shown). Vcmax, Jmax, and Rd were estimated by using nonlinear least squares regression to calculate the values of these parameters that best fit the equations of the von Caemmerer and Farquhar (1981)
photosynthesis model (Harley et al., 1992
; Wullschleger, 1993
). Measured values of Vcmax and Jmax were adjusted to a common temperature of 25°C following Harley et al. (1992)
and Leuning (1997)
.
Diurnal measurements of A and E were made on three plants each of R. ursinus and R. discolor, alternating between the species, on 6 d during May and early June 2000. Measurements were made on each plant approximately every 2 h from 0630 to 1830. Temperature and vpd within the leaf cuvette were allowed to vary with ambient conditions. Instantaneous water-use efficiency was calculated as A/E (in micromoles of CO2 per millimoles of H2O) for each measurement.
Leaf analyses
Following field measurements, each leaf was collected, placed in a plastic bag, and kept in cold storage until laboratory analyses were performed, which was typically within 48 h of collection. Leaf area was determined using a video image recorder and AgVision software (Decagon Devices, Pullman, Washington, USA). Leaves were then dried for 48 h at 65°C and mass was measured to the nearest 0.01 g immediately upon removal from the oven. Specific leaf area (SLA, in square centimeters per gram) was calculated as area per unit mass for each leaf.
Dried leaves of all four species collected from the McDonald-Dunn Forest and of R. discolor and R. ursinus collected from three other sites were ground for elemental analysis. Leaf N and carbon content (Com) were measured on a subsample of ground material from each leaf using a NC2500 elemental analyzer (CE Instruments, Milan, Italy). Instantaneous PNUE (in micromoles of CO2 per mole of N per second) was calculated as Amax per leaf N. The construction cost (CC) of leaf tissue (grams of glucose necessary to synthesize 1 g leaf tissue) was calculated according to the equation developed by Vertregt and Penning de Vries (1987)
The 13C (in parts per thousand) for leaves of R. ursinus and R. discolor was measured on 2.0 ± 0.1 mg ground subsamples of leaves collected from the McDonald-Dunn Forest and from the three other sites in western Oregon using a Finnigan MAT stable isotope mass spectrometer (Bremen, Germany) at the Idaho Stable Isotope Laboratory (Moscow, Idaho). The stable carbon isotope composition was calculated as
 | (2) |
). In plant tissues, the values of 13C/12C are less than those of the standard and therefore, 13C is negative. When comparing 13C values between plant samples, those that are less negative have relatively more 13C, which indicates higher WUE (Farquhar, O'Leary, and Berry, 1982
; Johnson et al., 1990
; Knight, Livingston, and Van Kessel, 1994
).
Discriminant analysis
Discriminant analysis was used to examine whether the measured photosynthetic characteristics may be used to distinguish between invasive and noninvasive species. This analysis was performed for these data by first grouping each of the four species into either an invasive or a noninvasive species category. Then, a classification function was developed for each of the two categories using Amax, Jmax, Vcmax, SLA, and leaf N and leaf CC on a leaf area basis for individual plants to calculate a discriminant score. Integrated and instantaneous WUE data were available for only two species, so those parameters were used in a subsequent discriminant analysis along with the ratio of A to Rd and PNUE to classify individuals of R. ursinus and R. discolor. Using the classification functions developed for each group, an individual case was grouped into the category for which its discriminant score was highest. An approximate F test was calculated from a transformation of Wilks' lambda to test the equality of group centroids and, therefore, test the distinctness of groups (SYSTAT, 1999
). An F-to-remove statistic can be used to determine the relative importance of the input variables of the classification function for predicting group membership (SYSTAT, 1999
). To examine this discriminant analysis graphically, Mahalanobis distances from the category centroid were calculated for each case given the posterior probability of group membership. The pair of these distances was then plotted for each case, where similar data points (i.e., those that are grouped in the same category by the discriminant analysis) will have a similar pair of distances and will therefore be plotted together as a group (SYSTAT, 1999
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In both of the invasive Rubus species, SLA was lower than the noninvasive species (F3,70 = 27.34, P < 0.0001; Table 1). The CC per gram of leaf was very similar among all four species (F3,50 = 0.136, P = 0.94; Table 1). However, on an area basis, values of CC were higher in the invasive species (F3,50 = 3.165, P = 0.03; Table 1). Leaf N was significantly different among the four species at the McDonald-Dunn site (F3,50 = 3.54, P = 0.02; Table 1). The noninvasive R. ursinus had the highest leaf N of the four species, although its leaf N was not significantly higher than that of R. discolor. At the three other sites from which leaves were collected, R. ursinus had higher leaf N than R. discolor, and these differences were also not statistically significant (data not shown). Leaf N per unit leaf area was higher in the invasive species, although the values for the invasive R. discolor and noninvasive R. ursinus were not significantly different (F3,50 = 12.16; P < 0.001; Table 1).
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13C values of R. discolor further demonstrate that this species tends to have higher WUE than the noninvasive species (Fig. 6). At all four sites from which leaves were collected, R. discolor had less negative 13C values, indicating higher integrated WUE (randomized block ANOVA F1,45 = 5.50, P = 0.02).
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13C) were available for only these two species. Only two out of 36 cases were misclassified in this analysis; one noninvasive and one invasive case (data not shown). The most important variable in discriminating between the two species was instantaneous A/E (F-to-remove = 4.81). In spite of the misclassifications, there was a good discrimination between R. discolor and R. ursinus when using these variables of resource capture efficiency as inputs (approximate F4,43 = 8.3511, P < 0.0001). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In addition to having higher Amax, leaves of the invasive species remained on the canes for longer, enabling them to have an extended period of carbon gain. Second-year foliage of the noninvasive R. ursinus senesces in early July, while that of both invasive species does not senesce until September or October. Furthermore, unlike the three other species in this study, the noninvasive R. leucodermis completely sheds all first-year foliage in the fall and therefore has no net carbon gain during the winter. The higher photosynthetic capacity maintained over a longer period of the year enabled these invasive species to fix significantly more carbon over their two-year lifespan than the noninvasive species (McDowell and Turner, in press). This accumulation of carbon may be translocated to the perennial roots following cane senescence and stored for future cane and fruit production.
Cost of resource capture
While leaf CC per unit dry mass was similar among the Rubus, SLA was lower in the invasive species for foliage collected from the same light environment in the same sites as the noninvasive species, resulting in the higher CC per unit leaf area for the invasive species. Therefore, the invasive species allocated a greater amount of carbon to leaf tissue per unit of light-absorbing surface. These results contrast with those from a study of leaf characteristics of invasive and noninvasive species growing along pond banks in New York (Nagel and Griffin, 2001
) and from two Hawaiian studies comparing groups of invasive and noninvasive species (Baruch and Goldstein, 1999
; Durand and Goldstein, 2001
). These other studies found that SLA was generally higher and area-based leaf CC was lower in invasive species than noninvasive species. In one of these studies, Baruch and Goldstein (1999)
compared 34 invasive and noninvasive species from different genera in Hawaii, including one invasive and one noninvasive species of Rubus. In contrast to the general pattern of SLA for species in that study, the SLA of the invasive Rubus was lower than that of the noninvasive, similar to the patterns observed for Rubus in this study. These results highlight the fact that comparisons of average patterns across invasive and noninvasive species of different genera does not necessarily lead to generalizable conclusions regarding mechanisms of success for particular invasive species.
Although the SLA results from this study were not expected, the results for leaf N on a leaf area basis are consistent with the higher Amax observed for the invasive species. For a given N concentration, plants with a low SLA will have higher N per unit leaf area. Most leaf N is allocated to photosynthetic pigments and enzymes, and, therefore, a higher N per leaf area should translate into higher photosynthetic capacity, as was observed for invasive as compared with noninvasive Rubus. However, studies examining the relationship among SLA, leaf N, and Amax across species show that species with low SLA generally have a lower PNUE and a smaller change in Amax per unit leaf N (Field and Mooney, 1986
; Reich and Walters, 1994
; Reich, Ellsworth, and Walters, 1998
). The invasive species used in this analysis deviate from this pattern by having high Amax per unit investment in leaf N in spite of low SLA, suggesting that invasive species may have different combinations of leaf traits than those plant species considered noninvasive.
The low SLA of the invasive species may also have aided in increasing WUE. Thicker, denser leaves (i.e., lower SLA) increase the distance through which water must diffuse to leave the leaf, leading to water conservation (Van den Boogaard and Villar, 1998
). Therefore, the thicker leaves of the invasive Rubus may have contributed to their greater integrated and instantaneous WUE. Although the value of 13C varied within each species across the sites from which samples were taken, this level of variation is commonly observed with changes in elevation and precipitation for a given species (Marshall and Zhang, 1994
; Panek and Waring, 1997
). The relative pattern of greater WUE for the invasive species held across all sites, indicating that WUE may be an important contributing factor to the success of this invasive Rubus species. This same pattern of low SLA and high WUE has been observed for an invasive dune grass as compared with a closely related noninvasive species in northern California, where water conservation is also likely to be important for invasive plant success (Pavlik, 1983
). In this study, discriminant analysis identified A/E (instantaneous WUE) as a powerful variable for distinguishing between the invasive and noninvasive Rubus species, providing further support that WUE may be an important contributing factor to invasive Rubus success in the PNW.
Another indicator of the carbon costs of resource gain is the relationship between Amax and Rd. All species exhibited a positive relationship between these two values, indicating a trade-off between rates of Amax and respiration costs. Across all ranges of Rd, the Amax values of the invasive species were higher than those of the noninvasive species. Therefore, the respiratory trade-off to high net photosynthetic rates is lower in the invasive Rubus relative to the noninvasive species. These results are consistent with those of another study examining the relationship between A and Rd in invasive and noninvasive plant species of different genera (Pattison, Goldstein, and Ares, 1998
).
The high values of PNUE in the invasive R. discolor in conjunction with high instantaneous rates of WUE demonstrates that this species is able to assimilate carbon at a relatively lower nitrogen and water investment than noninvasive R. ursinus. However, plants typically exhibit a trade-off between WUE and PNUE (Van den Boogaard and Villar, 1998
). That is, plants that achieve high WUE by closing their stomata may be expected to have high leaf N allocated to photosynthetic enzymes in order to maintain high A under a reduced supply of CO2. However, if high WUE is obtained without reduced stomatal conductance, then the trade-off between WUE and PNUE may not be observed (Hikosaka et al., 1998
; Van den Boogaard and Villar, 1998
). Stomatal conductance of R. discolor remains high relative to that of R. ursinus throughout diurnal and seasonal periods of drought (McDowell and Turner, in press). Therefore, the WUE observed in R. discolor is probably due to its high photosynthetic capacity and not due to reduced stomatal conductance. The maintenance of stomatal conductance through drought by the invasive Rubus may relate to its root allocation. Roots of R. discolor can descend more than 1.5 m into the soil, while those of the R. ursinus are relatively shallow and remain in the upper 0.5 m of soil (personal observation). Therefore, R. discolor may be able to access water that is unavailable to R. ursinus and therefore leave its stomata open throughout periods of high vpd. Analysis of R. discolor in Europe shows that it maintained high WUE, as inferred from 13C, when exposed to a variety of drought treatments, and this was apparently correlated with its high ratio of root to shoot biomass and ability to access soil water at the expense of neighboring plants (Fotelli et al., 2001
). Therefore, WUE is a trait that is important to the success of R. discolor, even in its native range.
Discriminant analysis
The discriminant analysis summarizes the data from this study. The characteristics measured in this study proved to be very powerful in discriminating between invasive and noninvasive Rubus and, therefore, may be important factors contributing to their success. In particular, Amax and A/E were identified as the most powerful variables in the discriminant analysis. This combination of high photosynthetic capacity and high photosynthetic rates relative to water loss may be critical to the acquisition of carbon and tolerance of summer drought in the PNW for these species, leading to their high rates of growth and reproduction. While observations of other invasive species have also identified lower resource costs of photosynthesis relative to co-occurring noninvasive species, the particular combination of traits associated with invasive plants appears to vary with species and environmental conditions. This study, to my knowledge, is the first to use discriminant analysis to distinguish between physiological traits of invasive and noninvasive species. Further studies using discriminant analysis may help identify mechanisms of success for other invasive species or, if developed using a larger set of species, may prove useful for predicting invasiveness within particular environments.
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FOOTNOTES |
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2 Current address: University of California, Environmental Studies Department, Santa Cruz, California 92407 USA
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J. Huang, R. E. J. Boerner, and J. Rebbeck Ecophysiological responses of two herbaceous species to prescribed burning, alone or in combination with overstory thinning Am. J. Botany, May 1, 2007; 94(5): 755 - 763. [Abstract] [Full Text] [PDF]
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M. T. Brock and C. Galen Drought tolerance in the alpine dandelion, Taraxacum ceratophorum (Asteraceae), its exotic congener T. officinale, and interspecific hybrids under natural and experimental conditions Am. J. Botany, August 1, 2005; 92(8): 1311 - 1321. [Abstract] [Full Text] [PDF]
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 J. GULIAS, J. FLEXAS, M. MUS, J. CIFRE, E. LEFI, and H. MEDRANO Relationship between Maximum Leaf Photosynthesis, Nitrogen Content and Specific Leaf Area in Balearic Endemic and Non-endemic Mediterranean Species Ann. Bot., August 1, 2003; 92(2): 215 - 222. [Abstract] [Full Text] [PDF]
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= 0.05 level of significance
