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Ecology |
Département de biologie and Centre de Recherche en Biologie Forestière, Université Laval, Ste-Foy, Québec, Canada G1K 7P4
Received for publication May 4, 2001. Accepted for publication August 23, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: distribution limit • growth rates • latitudinal gradient • Liliaceae • overstory canopy closure • spring flowering plants • tree leaf phenology • Trillium
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Risser and Cottam, 1968
). Spring flowering plants such as Trillium erectum also rely on this period of open canopy to accumulate carbohydrate reserves for both future growth and reproduction, despite the fact that they keep their leaves over the summer (Lapointe, 1998
). Despite the dependence of many understory plant species on this high light period in early spring, the impact of overstory tree leaf phenology on understory plants have received little attention. A few studies have reported an advantage for early germinating tree species, which can profit from the first few weeks of high light conditions in early spring (Jones and Sharitz, 1989
; Jones et al., 1994
; Seiwa, 1998
). The success of some exotic shrubs in North America is attributed to their capacity to leaf out earlier than native shrubs (Harrington, Brown, and Reich, 1989
), with 27–35% of annual carbon gain in these shrubs occurring before overstory canopy closure. Within a forest, variation in tree leaf phenology across species affected the number of flowers and fruits produced by the understory shrub Staphylea bumalda (Maeno and Hiura, 2000
). To our knowledge, there are no reports on the impact of the variation in tree leaf phenology on spring flowering plant populations, but we expect these species to respond as strongly, if not more, than understory shrubs and tree seedlings to changes in the overstory leaf emergence phenology.
Tree leaf phenology varies among species, but also along latitudinal gradients (Lechowicz, 1984
). However, across taxa, common garden experiments show contradictory results on the impact of the site of origin on the date of leaf emergence. In sugar maple, genetic differences between populations only explain a small fraction of the variation in the date of leaf emergence (Kriebel and Wang, 1962
). Recently, Raulier and Bernier (2000)
developed a model, based on the number of chilling days and degree-days during winter and early spring, to predict the date of leaf emergence in sugar maple. This model predicts that leaf emergence occurs earlier with respect to snow melting in more northern sites due to the higher number of chilling days and the fact that fewer degree-days are required before leaf emergence. Earlier tree leaf emergence in more northern sites could affect the growth of understory species that do not show changes in the timing of emergence with respect to snow melting. This is most probably the case for early sprouting species that emerge as soon as the snow melts in early spring.
The objective of the present study was to determine weather T. erectum growth and reproduction were affected by the duration of the high light period in early spring. We followed three populations of T. erectum distributed along a latitudinal gradient in sugar maple forests. We monitored the differences in canopy closure along with T. erectum phenology, carbon allocation patterns, plant growth rate, and fruit characteristics in the different T. erectum populations. Differences in growth rate and reproductive capacity among these populations would support the hypothesis that tree leaf phenology plays a significant role in spring flowering species distribution at a local as well as at a regional scale.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), starting at the beginning of the T. erectum growing season, when the buds emerged from the soil, and ending when the overstory canopy closure was complete. This was repeated five times at each study site. For each photo, the presence of foliage at 100 intersection points in a 10.2 cm x 15.2 cm grid was noted. At each site, photosynthetic photon flux density (PPFD) in an adjacent clearing and under the overstory canopy (same positions where canopy closure photos were taken) was measured during the summer, on a sunny day, using a SunScan probe (Delta-T, Cambridge, UK).
In order to insure that differences in plant growth rate were not due to major differences in soil nutrient availability, soil nutrient concentrations were estimated at the three sites. Fifteen samples were collected at random from each site at the end of July. Samples were sieved through a 2-mm mesh then pooled into five samples. For total N, subsamples were ground then analyzed using the Kjeldahl procedure (Bremner and Mulvaney, 1982
). Extractable P, K, Ca, and Mg were analyzed following the Mehlich III procedure (Mehlich, 1984
).
Plant harvests
Once a week, over spring and summer 1997, eight reproductive plants from each of the study sites (Joliette, Québec City, and Hébertville) were harvested. Trillium erectum is a long-lived slow-growing species, and plants that produce flowers are at least 7 yr old (Patrick, 1973
). The plants were divided into roots, rhizome, stem, leaves, flower or fruit, and overwintering bud. Leaf areas were recorded using a leaf area meter (model 3100, LI-COR, Lincoln, Nebraska, USA). Stem lengths and the number of annual constrictions on each rhizome (Davis, 1981
) were also recorded. Each plant part was then dried separately at 70°C and weighed. Rhizome annual growth rate (in grams per year) was calculated as the rhizome dry mass divided by the number of annual constrictions. Specific leaf area (SLA, in square meters per kilogram) was estimated as the total leaf area divided by leaf mass. Initially, carbon allocation patterns were determined for each week. We then pooled the data for successive weeks that showed a stable pattern (4 wk in each site).
Fruit analysis
In the summer of 1997, fruit set ([number of plants with a mature fruit x 100]/number of flowering plants) was estimated from 40 flowering T. erectum plants within each site. Fruits were harvested at maturity, i.e., when they were easily detached from the pedicel. Seed set ([number of mature seeds x 100]/total number of ovules) and percentage of fertilized ovules ([number of mature seeds + number of aborted seeds] x 100/total number of ovules) were calculated as in Lapointe (1998)
. The carpels and seeds were then dried at 70°C and weighed.
Statistics
A one-way MANOVA was performed on the carbon allocation patterns of the three populations on arcsine-transformed data. Since the MANOVA showed that the overall carbon allocation pattern differed between species, one-way ANOVAs were then performed on each variable. The other morphological parameters, including fruit characteristics, were compared between populations using one-way ANOVAs. Some of the data were transformed (natural log) to meet normality requirements. An a posteriori Tukey test was used following a significant ANOVA result (P 
0.05). Chi-square test was used to compare fruit set between sites.
The soil temperature at the time of T. erectum emergence (week 0) was estimated from linear regressions using maximum daily soil temperature from the beginning of week 2 (first data points) to the end of week 7. Maximum daily soil temperatures at the three sites, from the beginning of week 2 to the end of week 7, were compared using a one-way ANOVA. Nutrient concentrations were also compared using one-way ANOVA on log-transformed data (for phosphorus and potassium) or on rank-transformed data (for magnesium).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1°C and warmer than Hébertville, the northernmost site, by 3°C at least until July. However, when time was expressed in terms of weeks of growth of T. erectum since bud swelling (week 0), we found that soil temperatures were similar between sites (F = 0.67; P = 0.518; Fig. 2B). Using linear regression of soil temperature as a function of weeks of growth of T. erectum, we estimated that the soil temperature at plant emergence was 6.7° ± 0.3°C (r2 = 0.78, P < 0.001).
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59 ± 19 µmol·m–2·s–1 in Joliette, 37 ± 29 µmol·m–2·s–1 in Québec City, and 26 ± 11 µmol·m–2·s–1 in Hébertville. The mean PPFD for adjacent clearings was 1606 ± 65 µmol·m–2·s–1. One-way ANOVA on ranks showed significant differences between understory PPFD at Joliette and at Québec City with Hébertville having an intermediate value (F = 6.01, P = 0.008). There were differences in the timing of canopy closure (>90% of complete closure) in relation to T. erectum growing season between the three sites (Fig. 3). In 1997, the canopy was closed 3 wk in Hébertville, 4 wk in Québec City, and 5 wk in Joliette, after the beginning of the T. erectum growing season. In 1998, the canopy was closed 2 wk after the beginning of the T. erectum growing season in Hébertville, but in the fourth week of the T. erectum growing season at the Québec City and Joliette sites. Thus, the time between the initiation of T. erectum development and complete canopy closure was consistently longer in Joliette and in Québec City than in Hébertville. The rate of canopy closure was relatively constant from one site to another and between years (similar slopes).
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Fruit characteristics also showed difference among the three T. erectum populations (Table 3). Fruit set ranged from 75% to 92.5%, but these differences were not statistically significant. Total fruit dry mass and carpel dry mass differed between the three sites, decreasing from the southernmost site to the northernmost site. Total fruit dry mass ranged from 128 ± 10 mg to 393 ± 34 mg. Mean seed mass was lower in Québec City than in Joliette and in Hébertville. Trillium erectum fruits from Joliette had a mean of 74 ± 6 seeds per fruit, while T. erectum fruits from Québec City and from Hébertville had a mean of 30 ± 3 and 25 ± 2 seeds per fruit, respectively. On the other hand, no difference was observed in seed set, which ranged from 53 ± 4% in Québec City to 64 ± 3% in Joliette, nor in the percentage of fertilized ovules, which ranged from 63 ± 3% in Québec City to 71 ± 3% in Joliette (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Bazzaz and Bliss, 1971
). Soil temperatures at the beginning of the T. erectum growing season were similar between sites, and there appears to be a soil temperature threshold of 7°C for bud burst in this species. Others have reported a close relationship between Trillium development and completed snow melt, but none have reported specific soil temperatures (Vézina and Grandtner, 1965
; Irwin, 2000
).
The overstory maple sugar canopy started to close later in the coolest region, but the speed of canopy closure was similar over all regions. On a broader scale, Acer saccharum leaf development also followed a latitudinal gradient (Leith, 1974
). The initiation of tree leaf development has been related to the number of degree-days prior to leaf emergence (Lechowicz, 1984
). However, as leaf emergence occurs at cooler temperatures in northern sugar maple populations, other factors than degree-days alone control leaf emergence in this species. These differences could be under genetic control (Kriebel, 1957
), although Raulier and Bernier (2000)
recently proposed that a combination of chilling days and warming days could explain the date of leaf emergence in sugar maple populations. Therefore, it appears that both Acer saccharum leaf emergence and spring flowering plant shoot emergence are controlled by temperature. But, while spring flowering plants appear to maintain the same soil temperature threshold irrespective of latitude, A. saccharum has adapted to cooler environments and requires fewer degree-days to initiate bud burst.
Before canopy closure, understory plants receive more light daily and have higher photosynthetic rates (Sparling, 1967
; Taylor and Pearcy, 1976
; Gill, Amthor, and Bormann, 1998
). As canopy closure occurs earlier in the development of spring flowering plants in northern populations, there is a south to north gradient in the duration of the high light period and thus of the high photosynthetic rates in the understory. This high irradiance period plays a crucial role in carbon reserve storage in T. erectum (Lapointe, 1998
). Trillium erectum accumulates carbon in its rhizome for the next year's growth during the first weeks in spring. During the same period, it also accumulates carbohydrates in its stem and these carbohydrates are used for fruit development once the overstory canopy has closed (Lapointe, 1998
). Many spring plants accumulate their reserves during the high light period in spring. Risser and Cottam (1968)
found that starch, which is the primary storage material, accumulates rapidly in spring prior to overstory canopy closure in maple forest spring ephemerals, such as Erythronium spp. and Dicentra spp. Seiwa (1998)
showed that an understory tree Acer mono gains 79% of its annual dry mass before overstory canopy closure. Therefore, the length of time available to understory plants for carbon gain is largely determined by the foliar phenology of overstory trees in deciduous forests (Seiwa, 1998
), and summer PPFD levels most probably do not strongly influence plant annual growth rates nor fruit production, a conclusion that concurs with results of Maeno and Hiura (2000)
for Staphylea bumalda.
Northern T. erectum plants were smaller, and their annual growth rate, measured by the increase in rhizome biomass per year, was also lower. Data from Chmielewski and Ringius (1987)
and Davis (1981)
support these observations. Aerial biomass of T. erectum is almost two times greater in a population from West Thornton, New Hampshire compared to a population from southern Ontario. Since plants from southern sites have a longer period of high irradiance, they can fix more carbon, and this translates into an increase in rhizome annual growth rate and an increase in carbon allocated to the overwintering bud. The duration of the high light period in the spring is variable from year to year (Fig. 2) and might induce the variability in annual growth rate observed in spring flowering species such as Erythronium americanum (Muller, 1978
).
Two other abiotic factors, spring soil temperatures and nutrient availability, could determine the presence and abundance of spring flowering species (Rogers, 1982
). There were similar soil temperatures at the three sites for the first 8 wk of T. erectum growth. Most of the plant growth has occurred by then, including carbohydrate accumulation (Goryshina, 1972
; Lapointe, 1998
). Overwintering buds developed during the seventh week of growth for Hébertville population and during the tenth week of growth for Joliette population (data not shown). Furthermore, nonfruiting plants senesce in late June (L. Lapointe, personal observations), which also suggests that most growth occurs early in the season, when soil temperatures are similar among locations.
Overall, soils at the more southern site were not much richer than soils at the more northern sites. Although nutrient requirements are not known for Trillium species, it appears from their nitrogen/phosphorus ratios that vernal herbs are more limited by nitrogen than by phosphorus (Anderson and Eickmeier, 1998
). Soil phosphorus concentrations higher than 20 mg/kg are considered high, while concentrations lower than 3 mg/kg are considered limiting in natural habitats (Binkley and Vitousek, 1991
). As all three sites had concentrations above 3 mg/kg, phosphorus was not limiting. In relation to potassium, a fertilization study using Claytonia virginica showed that both belowground and aboveground potassium concentrations did not increase following fertilization (N-P-K), while nitrogen and phosphorus concentrations did (Eickmeier and Schussler, 1993
). Therefore, nitrogen is probably the most limiting nutrient for the growth of flowering species such as Trillium, and as soil nitrogen concentration was similar across all sites, nutrient availability was not an important factor in the differences in growth rates of the T. erectum populations.
Specific leaf area (measured in square meters per kilogram) gives an indication of the leaf thickness that within species is associated with the PPFD at the time leaves developed (Boardman, 1977
). Specific leaf area increased in T. erectum in a south–north gradient, reflecting the fact that northern plants completed leaf development after canopy closure, thus under lower PPFD. There are other parameters that also suggest stronger shade acclimation in the more northern populations of T. erectum. A higher percentage of carbon allocated to leaves is usually associated with shade acclimation (Björkman, 1981
). Stem height and percentage of carbon allocated to stem were higher in northern populations of T. erectum, which also suggests a lower light environment during plant development (Robison and McCarthy, 1999
). Therefore, light conditions during plant development appear to influence leaf morphology and carbon allocation patterns in T. erectum.
There were differences in fruit size and seed number among T. erectum populations. These differences in allocation to reproduction for T. erectum from different locations were not related to differences in pollination success, as fruit and seed set as well as the percentage of ovules fertilized did not differ between sites. Smaller fruits were associated with a lower carbon allocation to reproduction in more northern populations. Chmielewski and Ringius (1987)
also found that reproductive effort decreased among populations of T. erectum from southwest to northeast. Hickman (1975)
suggested that larger plants can allocate more resources to reproduction than smaller plants. However, Kawano, Ohara, and Utech (1986)
and Chmielewski and Ringius (1987)
found that for T. erectum and T. grandiflorum, an increase in plant biomass was related to a decrease and not to an increase in reproductive effort. Within populations, we did not find statistically significant correlations between the percentage of carbon allocated to the fruit and the total plant biomass, except for the Québec City population (r2 = 0.37; P = 0.02). Therefore, the difference in reproductive effort between the three T. erectum populations was probably due to differences in carbon availability caused by differences in the length of the high light period in the spring.
Differences in annual growth rate and in allocation to reproduction between T. erectum plants from different latitudes strongly suggest that the length of the high light period in spring, prior to canopy closure, is very important for the survival of spring flowering plant populations, even for the species that maintain leaves for most of the summer. The length of the high irradiance period may explain the northern distribution limit of some spring flowering plants such as T. grandiflorum, which initiates growth in the spring slightly after T. erectum. Spring flowering communities are much more diverse in the south (Rogers, 1982
), and the results of the present study strongly suggests that this could be due to latitudinal differences in tree leaf phenology. On a local scale, variation in flushing date between tree species might explain part of the variation in understory spring community among deciduous forest ecosystems. Further studies in which canopy closure is experimentally manipulated as well as reciprocal transplants are needed to test this hypothesis.
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FOOTNOTES |
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2 Author for reprint requests (FAX: 418-656-2043; Line.Lapointe{at}bio.ulaval.ca
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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