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0 Département de biologie and Centre d'études nordiques, Université Laval, Sainte-Foy, Québec, Canada G1K 7P4
Received for publication August 17, 1999. Accepted for publication March 28, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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20 g sea salt/L. However, this inhibiting effect was reversible: seeds from the salt treatments germinated readily after being washed in distilled water. Though seedling emergence was diminished at low salinity levels, postemergence survival was little affected. Plant growth was reduced, but net carbon assimilation rate was not affected by high salinity levels. Increased root respiration and respiratory costs associated with salt tolerance might have contributed to lower C accumulation at higher salinity levels. All developmental processes considered are thus negatively affected by substrate salinity, with potentially significant consequences on population abundance and distribution in salt marshes. Yet, the tolerance of this species to high salinity levels after seedling emergence is remarkable. Seed germination represents a major bottleneck in the species life cycle, potentially controlling local distribution and abundance in the natural habitat.
Key Words: Aster laurentianus • net carbon assimilation rate • plant growth • plant survival • salinity • seed germination • seedling emergence • water use efficiency
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Barbour and DeJong, 1977
; Ungar, 1987
; Bertness, Gough, and Shumway, 1992
; Sánchez, Otero, and Izco, 1998
). High salinity decreases substrate water potential and thus restricts water and nutrient uptake by the roots; high salinity may also cause ionic imbalance and toxicity in plants (Larcher, 1995
; Lambers, Chapin, and Pons, 1998
). The detrimental effects of salinity on plants may also vary with developmental stage (Adam, 1990
). Seed germination, seedling emergence, and early survival are particularly sensitive to substrate salinity (Mayer and Poljakoff-Mayber, 1989
; Mariko et al., 1992
; Baldwin, McKee, and Mendelssohn, 1996
; Katembe, Ungar, and Mitchell, 1998
; Williams, Meads, and Sauerbrey, 1998
). Often, growth and survival following emergence are not affected by low and moderate salinity levels (Baldwin and Mendelssohn, 1998
), although reproduction frequently is reduced even by low salt concentrations (Waisel, 1972
). However, high substrate salinity may be as (Poljakoff-Mayber et al., 1994
) or more (Ungar, 1996
) detrimental to plants in their early growth stages than to seeds.
Salt marshes are very dynamic systems with frequent and significant fluctuations in salinity and water level (Paskoff, 1985
). Disturbances as a result of wrack deposition and sedimentation are also significant in salt marshes (Brewer, Levine, and Bertness, 1998
; Pennings and Richards, 1998
). At higher latitudes, ice abrasion and glacial sedimentation also are common agents of disturbance. Because substrate salinity in coastal marshes varies through the growing season in relation to weather conditions and tidal activity (Adam, 1990
), there is a high probability of interactions between the temporal pattern of substrate salinity and plant phenological development. Such interactions are likely to affect plant population abundance and distribution in coastal marshes, particularly for annuals that must necessarily go through the germination and establishment phases every year.
Aster laurentianus is an annual plant, endemic to the Gulf of St. Lawrence (Houle, 1988
). It is considered a vulnerable species by the Committee on the Status of Endangered Wildlife in Canada (Houle and Haber, 1990
). It is present in New Brunswick, Prince Edward Island, and Québec, although most of the known populations of the species are found on Îles-de-la-Madeleine, in Québec (Gagnon et al., 1995
). There, A. laurentianus typically occurs in salt marshes at the periphery of shallow lagoons, forming a more or less well-defined band (from 
50 to 200 cm wide), immediately above the mean summer water level. Interstitial water salinity is variable among sites, but it can reach values of 15–20 g/L and more locally (G. Houle, personal observation). However, as a result of evaporation, substrate salinity at the surface may be much higher, with significant effects on seed germination and seedling emergence. Although A. laurentianus has been described as a halophyte, the species tolerance to salinity has yet to be estimated. Here, we present the results of a study of the effect of substrate salinity on different processes (i.e., germination, emergence, and growth) in the life cycle of A. laurentianus. We consider a broad range of salinities, which includes the extremes of shallow pools and exposed substrates, to determine how salinity limits the species distribution within the salt marsh habitat.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The fruit is an achene that bears a pappus. The fruits are mature by the middle of September and appear to be dispersed mostly by wind, although the pappus-bearing fruits of several Asteraceae are known to have good buoyancy in water (Huiskes et al., 1995
). Plant height and the degree of stem ramification are relatively plastic because at high densities plants are 10–15 cm high and their stem is mostly simple, but at low densities, plants may reach 40 cm in height and bear numerous branches (Boudreau and Houle, 1998
).
Seed material
On 19 September 1997, mature inflorescences were collected from 50 Aster laurentianus individuals in a population at Havre-aux-Basques, Îles-de-la-Madeleine (Québec, Canada). Achenes were kept at 5°C until the beginning of the experiments.
Germination
Twenty-five achenes were placed in petri dishes on two layers of filter paper wetted with a saline solution. The salinity levels tested were 0, 10, 20, 30, and 40 g sea salt/L, with ten petri dishes per salinity level. Dishes were sealed with Parafilm® and placed in a germination cabinet, under a 14-h photoperiod, at representative night and day temperatures (15°C and 25°C, respectively) during the period of germination in the natural habitat. Every day, for a 30-d period, dishes were inspected and germinated seeds were counted and removed. After 30 d, ungerminated seeds from each of five dishes per salinity treatment were washed thoroughly with distilled water and then put into petri dishes to germinate on two layers of filter paper wetted with distilled water. Dishes were put into a germination cabinet under conditions similar to those described above. Seed germination was recorded regularly for another 30-d period.
Data for percentage germination for the first 30-d period (under saline conditions) and for total percentage germination (for the whole 60-d period) were analyzed, after arcsine transformation, with one-way analyses of variance (ANOVAs). Differences between treatment means were determined with LSD (least significant difference) tests when the ANOVAs indicated that there were significant differences.
Emergence
Ten trays, 26 cm wide x 52 cm long x 5 cm deep, were filled with fine sand and placed on two benches in a greenhouse. Plastic panels were inserted into the sand to divide each tray into five sections. Twenty-four achenes were uniformly spread over the surface of each section and then covered with 2 mm of sand. Once a week (on Mondays), the trays were soaked in a nutrient solution prepared from a complete commercial fertilizer (20-20-20, N-P-K) and containing 0.4 g N/L. On Tuesdays, Thursdays, and Saturdays, the trays were soaked in a 10-g sea salt/L saline solution. To create a gradient of substrate salinity in the trays, a given section was watered with either 400, 300, 200, 100, or 0 mL of tap water after the trays had soaked in the saline solution (salinity levels 0, 1, 2, 3, and 4, respectively). On Wednesdays and Fridays, the trays were soaked in tap water and, on Sundays, they were given tap water from above so that a salt crust would not develop. The 10 g sea salt/L solution we used corresponds to the maximum salinity level at which seeds could germinate in the germination experiment (see Results, below) and thus to the highest salinity level the emerging seedlings would likely be exposed. Over 24 h, temperatures in the greenhouse varied between 20°C (night) and 30°C (day). Two sodium vapor lamps (400 W, PL Light System Canada), assuring a minimum PAR (photosynthetically active radiation) of 100 µmol·m-2·s-1 were used to extend the photoperiod to 14 h.
Every day, for a 44-d period, the trays were inspected for seedling emergence. Seedlings were individually marked and followed until the completion of the experiment. The experiment was stopped after seedling emergence had ceased for three consecutive days. Then, a sample of sand was taken from each section of each tray and substrate salinity was measured with a conductivity meter (M90, Corning Inc., New York, USA). Nine cubic centimetres of dry substrate (15.34 g) were thoroughly mixed with 27 mL of deionized water several times over a 1-h period prior to taking measurements. Because it took 3.84 g of water to saturate 9 cc of the substrate, the salinity we measured was that of a solution diluted 7:1. The salinity values we report are adjusted for this dilution.
The total number of emerged seedlings, percentage seedling mortality over the experimental period (arcsine transformed), and substrate salinity were analyzed in randomized complete block design ANOVAs. When the results indicated that there were significant differences among salinity levels, LSD tests were used to identify specific differences between treatment means.
Growth
Fifty achenes were placed on two layers of filter paper wetted with distilled water, in each of 20 petri dishes. The dishes were sealed with Parafilm® and placed in a germination cabinet at alternating temperatures of 13°C (night) and 19°C (day) under a 14-h photoperiod. After 2 wk, seedlings of similar size (cotyledon stage) were individually transplanted into 500-cm3 pots filled with fine sand. Five pots were randomly placed in each of 12 trays (i.e., blocks) on two benches in a greenhouse. Within each tray, seedlings were randomly assigned to one of five salinity treatments: 0, 10, 20, 30, and 40 g sea salt/L. These levels were chosen to reflect field substrate salinities during the July–September period when A. laurentianus plants realize most of their growth.
Temperatures in the greenhouse were set at 20°C (night) and 30°C (day) and the photoperiod was maintained at 14 h (as for the Emergence experiment, see above). After 8 wk of growth, the photoperiod was reduced to 10 h to induce flowering. Plants were allowed to acclimate to the sand medium for 4 wk before the beginning of the experiment. During that period, plants were watered once a week with 20 mL of a complete nutrient solution containing 0.4 g N/L, from a commercial 20-20-20 fertilizer (N-P-K); on the other days, they were watered with tap water.
During the experimental period, each plant continued to receive 20 mL of the nutrient solution once a week (on Mondays). On Wednesdays, Fridays, and Sundays, each pot was watered from above with 47 mL of tap water. Summed over 4 wk, this quantity of water is equivalent to the monthly precipitation recorded at the Îles-de-la-Madeleine during the summer period. On Tuesdays, Thursdays, and Saturdays, the pots were soaked in the appropriate saline solution. Excess water or solution was allowed to drain from the pots.
Measurements of net carbon assimilation (A), transpiration (E), and stomatal conductance (gs) were taken with a LCA-4 (ADC Ltd., Hoddesdon, UK) infra-red gas analyzer on plants representing the 0, 20, and 40 g sea salt/L treatments. When these measurements were taken, plants were then in their 6th wk of treatment (or 10th wk of growth).
After a total of 11 wk of growth, plants were harvested. Biomass was divided into roots, stems, leaves, and reproductive tissues (inflorescences and bracts). They were dried at 70°C for 36 h and weighed. For plants of six randomly chosen blocks, fresh leaf area was measured with a leaf area meter (CI-202, CID Inc., Vancouver, Washington, USA). For three randomly chosen blocks, substrate salinity was also measured as above.
The variables total biomass, total leaf area, number of inflorescences, root mass ratio (RMR, root mass divided by total biomass), stem mass ratio (SMR, stem mass divided by total biomass), leaf mass ratio (LMR, leaf mass divided by total biomass), reproductive mass ratio (RR, reproductive mass divided by total biomass), A, E, gs, and water use efficiency (A/E) were analyzed in randomized complete block design ANOVAs. All ratios were arcsine transformed for analysis. Multiple-comparison tests (LSD) were used to identify differences among treatment means when the ANOVAs indicated that there were significant differences. All statistical tests were done with SAS version 6.12 (SAS Institute Inc., Cary, North Carolina, USA).
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RESULTS |
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Emergence
Substrate salinity (total salts) differed significantly among treatments (P = 0.0001): it was 0.231 ± 0.028 g/L, 0.301 ± 0.028 g/L, 0.602 ± 0.077 g/L, 1.939 ± 0.245 g/L and 5.250 ± 0.581 g/L for levels 0, 1, 2, 3, and 4, respectively (all significantly different from each other at P 
0.05; protected LSD test). Since 5.25 g/L corresponds to a salinity treatment of 10 g sea salt/L (see Materials and Methods), a linear interpolation between the lowest and the highest levels provides an estimate of 0, 0.1, 0.7, 3.3, and 10 g sea salt/L for our levels 0, 1, 2, 3, and 4, respectively.
Total emergence (for a maximum of 24 plants/section) differed among salinity levels (P = 0.0011; Fig. 1): it was higher in the control (15.1 ± 2.1 plants/section) than in the other levels (for instance, 8.7 ± 1.5 plants/section, for salinity level 4). However, percentage mortality over the experimental period did not differ among salinity treatments (P = 0.3362): it ranged from 7 ± 2% for salinity level 1 to 20 ± 6% for salinity level 4.
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0.05, protected LSD test). Control plants (0 g sea salt/L) had a higher total biomass than those of the other salinity levels (P = 0.0035; Fig. 2). They also had a higher root (161%), stem (175%), and leaf mass (152%). Total leaf area also differed among treatments (P = 0.0009; Fig. 2): for the control plants, it was 177 ± 20 cm2 and for the other treatments, it varied from 90 ± 13 cm2 to 122 ± 8 cm2. The number of inflorescences per plant did not differ among salinity levels (P = 0.3746; Fig. 2), although it varied from 2.8 ± 1.5 (for 40 g sea salt/L) to 5.2 ± 1.9 (for 30 g sea salt/L). Specific leaf area, root mass ratio, leaf mass ratio, and reproductive mass ratio did not vary among treatments (all P > 0.05), however stem mass ratio was higher for the control plants than for those of the 30 and 40 g sea salt/L treatments (P = 0.0227; Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), seed germination being the most, and seed and plant survival the least sensitive processes.
Germination
Germination of A. laurentianus seeds was considerably reduced at the salinity level of 10 g sea salt/L and was completely inhibited by levels of 20 g sea salt/L and higher. A negative effect of salinity on germination has been reported for several halophyte species (e.g., Boorman, 1968
; Khan and Ungar, 1984
; Ungar, 1987
). Such a response might be related to the inhibitory effect of the solution low osmotic potential and/or to ionic toxicity (Poljakoff-Mayber et al., 1994
; Katembe, Ungar, and Mitchell, 1998
). However, dormant seeds of A. laurentianus could survive high salinities without any carryover effect because they germinated rapidly when transferred to nonsaline conditions. This response suggests that the inhibitory effect is mostly osmotic and reversible, as found by Ungar (1978, 1996)
.
Emergence
In this experiment, the effects of salinity on both the seeds and very young seedlings were considered. The highest salinity level used (level 4) corresponded to the highest salinity level at which seeds of A. laurentianus could germinate in the germination experiment (i.e., 10 g sea salt/L) and, consequently, to the highest salinity level the young seedlings would be exposed. Yet, even at salinity level 1 (which was equivalent to a treatment of 0.1 g sea salt/L), emergence of A. laurentianus seedlings was significantly reduced. This result is similar to what Waisel (1972)
reported for several other halophytes, i.e., a high sensitivity even to low salinity levels. Remarkably, in our experiment, salinity level did not have a significant effect on the survival of those seedlings that did emerge. This suggests that once establishment is completed, A. laurentianus plants are relatively tolerant to substrate salinity.
Growth
Salinity reduced total plant biomass by negatively affecting root, stem and leaf mass, but not reproductive mass. However, reproduction had only begun when we ended the growth experiment. Thus, over time, lower biomass production might have resulted in a lower reproductive output, as reported by Ungar (1978, 1987)
. Reduced biomass as a response to increased substrate salinity is quite common in halophytes (Waisel, 1972
). In fact, a salinity of 1% is sufficient to cause a significant biomass reduction in several halophytes (Ungar, 1996
).
Among the different allocation ratios considered, only stem mass ratio was significantly reduced by salinity. The below- to aboveground biomass ratio increased from 0.37 ± 0.03 (control) to 0.45 ± 0.04 (40 g sea salt/L) with increases in salinity, indicating that root mass was less affected than stem and leaf mass combined, a somewhat unusual response for a halophyte (Waisel, 1972
; Greenway and Munns, 1980
). However, a reduced aboveground biomass (particularly leaf mass) is likely to contribute to a reduction in salt-induced water stress in plants through decreased transpiration (Kozlowski, 1976; van Loo, 1992
).
Net carbon assimilation rate (A) was not affected by salinity, although stomatal conductance and, consequently, transpiration, were lower at higher salinity levels. The lower biomass of salt-stressed plants was thus not associated with a lower A. This suggests that respiration, particularly root and maintenance respiration were significantly higher for the salt-stressed than for the control plants, resulting in lower C-accumulation (Wang, Showalter, and Ungar, 1997
; Epron, Toussaint, and Badot, 1999
). Water-use efficiency (WUE) was higher for plants exposed to higher salinities, suggesting an adjustment within the plant, such as stomatal control of water losses, to conserve water (Ayala and O'Leary, 1995
). Environmentally induced changes in specific leaf area (SLA, leaf surface/leaf mass) may also lead to changes in WUE (Stanhill, 1986
); however, in the present study, the higher WUE of salt-stressed plants was not associated with a lower SLA.
Conclusion
Although it is an annual, A. laurentianus does not appear to behave like a fugitive species (i.e., it is not restricted to disturbed microsites) in the salt marsh habitat where it grows. The high salinities typical of open, locally disturbed microsites (Bertness, Gough, and Shumway, 1992
) would not allow the seeds to germinate, although established plants would be able to grow and survive under these conditions. Seed germination appears to represent a bottleneck in the species life cycle, restricting the range of possible microsites that the species can occupy in its typical habitat. Interannual variations in climatic conditions may influence substrate salinity during the period of seed germination and, consequently, cause significant interannual fluctuations in population size. However, climatic extremes would have a smaller effect when they occur after seedling establishment.
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FOOTNOTES |
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2 Author for correspondence (e-mail address: gilles.houle{at}bio.ulaval.ca
).
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