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A mixed strategy in the annual endemic Aster laurentianus (Asteraceae)—a stress-tolerant, yet opportunistic species¹

Département de biologie, Université Laval, Sainte-Foy, Québec G1K 7P4, Canada

Received for publication January 24, 2002. Accepted for publication June 20, 2002.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Several environmental factors influence the distribution of plants in coastal salt marshes. Substrate salinity is among the major factors preventing several species from establishing near the water line. However, interspecific competition for light and nutrients is often significant in determining the upper limit of plants along the salt marsh gradient. In this study, we tested the effects of substrate salinity and light and nutrient availability on the performance of the annual Aster laurentianus (Asteraceae), an endangered species of eastern Canadian salt marshes. This species is typically found in a narrow band along the shores of shallow lagoons, cornered between the high water line and the dense, herbaceous community of the upper marsh. Low light availability was the most significant factor limiting plant performance. Salinity had little effect on A. laurentianus as, unexpectedly, did nutrient availability. Yet plants were able to absorb nutrients when these were made more available. Luxury consumption, the uptake of excess nutrients, may make sense for this annual plant because the habitat in which it grows is subject to frequent disturbances (e.g., sand accretion and salinity pulses) that may kill canopy species and release suppressed A. laurentianus individuals. These results suggest that interspecific competition for light may play a significant role in restraining A. laurentianus from the upper part of salt marshes. Luxury consumption may help the species to opportunistically take advantage of release from taller species, particularly towards the upper edge of the salt marsh gradient.

Key Words: light • luxury consumption • nutrients • salinity • salt marsh • stress

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Resource availability and abiotic conditions largely determine plant performance, abundance, and distribution (Harper, 1977 ). Along environmental gradients, resources and abiotic conditions change progressively and are believed to be responsible for community structure (Whittaker, 1967 ). For instance, in coastal salt marshes, plants are subjected to sediment and wrack deposition, wave abrasion, substrate salinity, flooding, and water-logging, the effects of which decrease with distance from the water line (Adams, 1963 ; Earle and Kershaw, 1989 ; Sánchez, Izco, and Medrano,1996 ; Brewer, Levine, and Bertness, 1998 ). Although plants may be excluded from the lower portion of the gradient, closer to the water line, because of their respective tolerance to these abiotic conditions, interspecific interaction such as competition may determine their upper limit on the gradient (Pennings and Callaway, 1992 ). Competition for light and nutrients have been proposed as significant in determining the upper limit of plants along salt marshes (Levine, Brewer, and Bertness, 1998 ; Brumbt, 2001 ).

A high competitive ability for light is often associated with a high relative growth rate (RGR) that allows for rapid resource monopolization (Poorter and Garnier, 1999 ). Species with a high RGR usually respond better than slow-growing species to increased resource availability (Fichtner and Schulze, 1992 ). However, fast-growing species tend to perform poorly when resources are scarce, often worse than slow-growing species (Shipley and Keddy, 1988 ). Plants adapted to nutrient stresses are usually slow growers and cannot opportunistically use nutrients to increase growth when these become more available (Chapin, 1980 ; Chapin, Schulze, and Mooney, 1990 ). Instead, they tend to store them in their tissues (luxury consumption) and use them only when nutrients become depleted in the soil. However, luxury consumption may also be favored when light limits growth. Indeed, in such a case, luxury consumption may allow a species to respond faster to increased light level following canopy disturbance.

Aster laurentianus Fernald is an annual plant, endemic to the St. Lawrence Gulf (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 only known from eastern Canada (New Brunswick, Prince Edward Island, and Québec), and the largest populations are at Îles de la Madeleine, Québec, Canada (Gagnon et al., 1995 ). Previous studies have suggested that competition for light in the adult stage and susceptibility to high substrate salinity at the seed and seedling stages may be significant factors controlling the distribution of the species into a narrow band along the shores of shallow lagoons where it typically occurs (Brumbt, 2001 ; Houle et al., 2001 ; Reynolds, Houle, and Marquis, 2001 ; Reynolds and Houle, 2003 ). However, in its habitat, A. laurentianus performance varies considerably and may be related to spatial heterogeneity in nutrient availability (Boudreau and Houle, 1998 ), as has been shown for other salt marsh species (Levine, Brewer, and Bertness, 1998 ).

In the present study, we determine the effects of substrate salinity and light and nutrient availability on A. laurentianus performance (whole-plant biomass and proximate fitness, i.e., total seed production). We hypothesized that interactions among these factors (e.g., salinity x light; salinity x nutrient) might restrict the species' performance and, potentially, explain its local distribution along shallow lagoons.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Study species
Seeds of A. laurentianus germinate from late May to early June, and vegetative growth proceeds until early August. Within any given population, plant height at maturity may vary from 5 to 40 cm (Boudreau and Houle, 1998 ). Small plants remain unbranched and usually bear only one terminal capitule, but larger plants become much ramified and may bear over 100 inflorescences. Flowering begins in early to mid-August, and mature infructescences are present on the plants from mid- to late September (Fernald, 1950 ). The fruit, an achene bearing a pappus, is wind dispersed but can also float in water.

At Îles de la Madeleine, A. laurentianus is typically found at the margins of shallow lagoons, above the mean summer water level. It has been suggested that wrack and sand deposition, wave abrasion, tidal movements, and high substrate salinity might preclude the presence of the species near the water edge. Actually, saline conditions have been shown to inhibit seed germination and reduce seedling survival (Houle et al., 2001 ). However, once established, A. laurentianus plants appear relatively tolerant to salinity although much less to shade (Houle et al., 2001 ; Reynolds, Houle, and Marquis, 2001 ). Interspecific competition for light might thus determine to a large extent the upper limit of the species on the shore (Boudreau and Houle, 1998 ). Indeed, taller plants less tolerant of the conditions prevailing near the water line, such as Carex paleacea, Solidago sempervirens, Sonchus spp., and Spartina pectinata, form a relatively dense canopy over shorter plants such as A. laurentianus, just a few meters away from the water line.

Seed material
Mature infructescences were collected in mid-September 2000 from approximately 25 plants in a population at the Havre-aux-Basques lagoon, Îles de la Madeleine. Achenes were kept at 5°C until the beginning of the experiment.

In late September 2000, five achenes were sown in each of 120 pots filled with washed sand (512 cm³). The pots were placed in a glasshouse under a 14-h photoperiod and soaked in deionized water daily, for a period of 4 wk. At the end of this period and prior to the beginning of the experiment, seedlings were thinned to one per pot.

Experimental design
Three factors were studied: photosynthetic photon flux density (PPFD, two levels), nutrient availability (three levels), and substrate salinity (two levels). Wooden frames were covered with either two layers of black fiberglass netting (shaded cages) or one layer of transparent plastic into which holes had been pierced (control cages). The lower 20 cm of the cages was left open to allow for air circulation. For each PPFD level, there were ten cages, each sheltering six randomly chosen pots. Cages were placed in a glasshouse in ten blocks, each containing the two PPFD levels. Minimum and maximum (night and day) temperatures in the glasshouse during the experiment were 15.2 ± 0.3°C and 26.8 ± 0.3°C, respectively (mean ± 1 SE). Four sodium vapor lamps (400 W, PL Light System Canada) assuring a minimum of 100 µmol · m^–2 · s^–1 were used to extend the photoperiod to 14 h as the experiment was done during the winter when the natural photoperiod was short. At the beginning of the experiment, PPFD was measured at the pot level in each of the 20 cages (under cloudy conditions).

Pots were watered on a 6-d schedule. On the first, third, and fifth days, the pots were soaked either in deionized water (0 g sea salt/L) or in a salt solution (5 g sea salt/L). On the second day, the pots were soaked in deionized water and, on the fourth day, the pots were watered from above with deionized water (to avoid salt accumulation at the surface of the sand). On the sixth day, the pots were soaked in a nutrient solution made of either 0.01, 0.1, or 1 g/L of 20–20–20 Plant-Prod Plus (Plant Products, Brampton, Ontario, Canada), a complete fertilizer, with both macro- and micronutrients.

After 7 wk of treatment, when the plants began to show signs of senescence, the experiment was terminated. Plants were taken out of their pots, and each root system was carefully washed in water. Plants were then separated into roots, stem, leaves, and reproductive tissues. For each plant, capitule number was determined and the number of achenes per capitule was counted on a random subset of capitules (one randomly chosen capitule for each ten capitules). From the number of achenes per capitule and the number of capitules per plant, the number of achenes per plant was estimated. Then, all biomass components (roots, stem, leaves, and reproductive tissues) were dried at 70°C for 36 h and weighed. Tissues were then milled and N, P, and K concentrations (in percentages) were determined (N and P: on Hitashi U1100, San Jose, California, USA; K: on Perkin Elmer 3300, Ueberlingen, Germany). Nitrogen, P, and K contents (in milligrams) were calculated as total biomass (in milligrams) x nutrient concentration (in percentages).

For five of the blocks, a sample of sand was taken from each of the pots and salinity was measured with a conductivity meter (M90, Corning, New York, New York, USA). Nine cubic centimeters of dry substrate were thoroughly mixed with 27 mL of deionized water several times over a 1-h period prior to taking measurements. Because it took ca. 4 cm³ of water to saturate 9 cm³ of substrate, the salinity we measured was that of a solution diluted 6.8 : 1. The salinity values we report are adjusted for this dilution.

Statistical analyses
Total biomass, number of capitules, number of achenes per capitule, and number of achenes per plant, and N, P, and K concentrations and contents were analyzed with split-plot design analyses of variance (ANOVAs). Photosynthetic photon flux density levels were the whole plot treatments and nutrient x salinity combinations were the subplot treatments (Montgomery, 2001). Biomass ratios (root, stem, and leaf ratios and reproductive effort) were also analyzed with split-plot design ANOVAs after an arcsine-square root transformation (Sokal and Rohlf, 1995 ). All analyses were carried out with SAS 6.12 (SAS Institute, Cary, North Carolina, USA). Initial PPFD values were compared with a randomized complete block design ANOVA.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Initial PPFD values (at midday, under overcast conditions) for the control and the shade treatment were 106.0 ± 5.6 µmol · m^–2 · s^–1 and 37.4 ± 5.0 µmol · m^–2 · s^–1, respectively (mean ± 1 SE, P 0.0001); these values are comparable to those recorded in the field under cloudy conditions, at Îles-de-la-Madeleine (Brumbt, 2001 ), along a gradient from the upper to the lower marsh. Substrate salinity differed significantly between salinity treatments (P = 0.0001), but not between PPFD (P = 0.8316) or among nutrient addition treatments (P = 0.1770). Salinity was 1.1 ± 0.1 g salts/L for the control and 8.9 ± 0.4 g salts/L for the 5 g sea salt/L treatment (mean ± 1 SE); these values represent the gradient of substrate salinity recorded in the field along the shores of shallow lagoons at Îles-de-la-Madeleine (Brumbt, 2001 ).

Total biomass was significantly affected by PPFD level (P 0.0001), but not by salinity (P = 0.9456) or nutrient addition levels (P = 0.8138; Fig. 1). Under full light, plants reached a biomass approximately eight times greater than that of shaded plants (overall mean ± 1 SE: 0.785 ± 0.055 g and 0.093 ± 0.010 g, respectively).

View larger version (36K): [in this window] [in a new window]   Fig 1. Total biomass of Aster laurentianus plants according to light, salinity, and nutrient treatments (means + 1 SE). White bars: 0.01 nutrient concentration; gray bars: 0.1 nutrient concentration; black bars: 1x nutrient concentration. Different letters indicate significant differences between light treatments

View larger version (20K): [in this window] [in a new window]   Fig. 2. Number of capitules per plant, of fruits per capitule, and of fruits per plant for Aster laurentianus according to light, salinity, and nutrient treatments (means + 1 SE). White bars: 0.01 nutrient concentration; gray bars: 0.1 nutrient concentration; black bars: 1x nutrient concentration. Different letters indicate significant differences between light treatments

View larger version (37K): [in this window] [in a new window]   Fig. 3. Nitrogen, P, and K concentrations and N, P, and K contents of Aster laurentianus plants according to light, salinity, and nutrient treatments (means + 1 SE). White bars: 0.01 nutrient concentration; gray bars: 0.1 nutrient concentration; black bars: 1x nutrient concentration

Contrary to our expectations, none of the two- or three-way interactions (light x salinity; light x nutrient; salinity x nutrient; and light x salinity x nutrient) were significant in the ANOVAs.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Higher PPFD enhanced all performance variables—total biomass, number of capitules, number of achenes per capitule, and number of achenes per plant. Higher PPFD decreased LR and, concomitantly, increased RR and RE (see also Olff, 1992 ). Unexpectedly, nutrient addition and salinity had no significant effect on overall plant performance, although higher salinity increased LR, but decreased RR. Nutrient concentration (N, P, and K) decreased with increasing PPFD, but increased with increasing salinity and nutrient availability. Yet N, P, and K concentrations remained relatively low (Thompson et al., 1997 ). Nutrient content increased with increasing PPFD, but mostly through the effect of PPFD on total biomass.

Reynolds, Houle, and Marquis (2001) showed that A. laurentianus relative growth rate (RGR) was quite low for an annual (0.08–0.12 d^–1) and was highly responsive to PPFD and salinity. However, the effect of PPFD and salinity on proximate plant fitness (seed output) was not determined in Reynolds, Houle, and Marquis' experiment. In the present study, we show that proximate plant fitness is relatively tolerant to moderate salinity stress, although highly sensitive to shading. Along the shallow lagoons of Îles-de-la-Madeleine, plant cover and substrate salinity vary inversely, salinity decreasing and plant cover increasing progressively with distance from the water line (Brumbt, 2001 ; Reynolds and Houle, 2003 ). Aster laurentianus response to PPFD and salinity may thus explain, at least in part, its distribution into a narrow band along lagoons. Competition for light may thus determine the species' upper limit on the shores (Brumbt, 2001 ), but substrate salinity, which inhibits seed germination, may preclude its presence close to the water line (Houle et al., 2001 ).

Nevertheless, within the zone that A. laurentianus occupies at the periphery of shallow lagoons, plant performance varies tremendously, small plants producing a single capitule and larger plants often bearing over 100 inflorescences (Brumbt, 2001 ). Although such variations may be related to fine scale heterogeneity in PPFD, spatial heterogeneity in nutrient availability may also influence proximate plant fitness (Robinson, 1994 ; Cui and Caldwell, 1997 ). However, we showed that A. laurentianus was exceptionally unresponsive to increased nutrient availability. Yet, plants were able to absorb nutrients when these were made available in larger quantities, although they were unable to "transform" them into new tissues.

Low RGR and inability to respond to increased nutrient availability are two characteristics of stress-tolerant plants (Grime, 1977 ; Shipley and Keddy, 1988 ; Lambers, Chapin, and Pons, 1998 ). Luxury consumption is a common phenomenon in such slow-growing plants that may use stored nutrients after soil reserves are exhausted or when conditions become less restrictive (Chapin, 1980 ). However, these slow-growing plants typically are perennials. Luxury consumption in an annual may make sense if the habitat it occupies is subject to frequent disturbances or pulse stresses (salinity pulses as a result of storms) that kill those more salinity-sensitive plants forming the canopy and, thus, release the suppressed "understory" plants, i.e., making the growth conditions less restrictive. Because branches can be produced at the base of each leaf, giving rise to secondary, tertiary, quaternary, etc., branches all terminated by a capitule, A. laurentianus may benefit from canopy disturbance when nutrients have been stocked. The higher nutrient concentration of our shaded plants is consistent with this scenario (see also Olff, 1992 ; Minotta and Pinzauti, 1996 ). Nutrient contents were significantly higher at the higher PPFD level, but essentially because of the effect of PPFD on total biomass. This suggests that full-light plants, although their nutrient concentration was lower, were still overall better at absorbing nutrients than shaded ones, a result consistent with the findings of other studies on herbaceous plants (Cui and Caldwell, 1997 ; Anderson and Eickmeier, 1998 ).

Spatial heterogeneity in soil nutrient availability is not likely to be responsible for the variability in A. laurentianus performance in the natural habitat, although it may modulate the plant response to increased PPFD as a result of canopy disturbance. Substrate salinity and PPFD, but not nutrient availability, may be major determinants of A. laurentianus distribution along the shores of shallow lagoons through their respective effects on seed germination and plant performance (Brumbt, 2001 ; Houle et al., 2001 ; Reynolds, Houle, and Marquis, 2001 ; Reynolds and Houle, 2003 ; the present study). Aster laurentianus thus appears to combine characteristics of both a stress-tolerant and an opportunistic species because of its ability to store nutrients and potentially use them when released from suppression.

	FOOTNOTES

 
¹ We thank M. Maurie for her technical assistance and L. Lapointe and two anonymous reviewers for their comments on an earlier version of this manuscript. We acknowledge the financial assistance of the Ministère de l'Environnement du Québec and the Natural Sciences and Engineering Research Council of Canada.

² Author for reprint requests (gilles.houle{at}bio.ulaval.ca) .

	LITERATURE CITED

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Houle, G. Articles by Valéry, S. Search for Related Content PubMed Articles by Houle, G. Articles by Valéry, S. Agricola Articles by Houle, G. Articles by Valéry, S.