AOBPreview originally published online on February 16, 2007
Annals of Botany 2007 99(4):723-734; doi:10.1093/aob/mcm007
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Local Adaptation Enhances Seedling Recruitment Along an Altitudinal Gradient in a High Mountain Mediterranean Plant
Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos–ESCET, Tulipán s/n. 28933 Móstoles, Madrid, Spain
* For correspondence. E-mail: luis.gimenez{at}urjc.es
Received: 20 October 2006 Returned for revision: 17 November 2006 Accepted: 12 December 2006 Published electronically: 16 February 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: Germination and seedling establishment, which are critical stages in the regeneration process of plant populations, may be subjected to natural selection and adaptive evolution. The aims of this work were to assess the main limitations on offspring performance of Silene ciliata, a high mountain Mediterranean plant, and to test whether local adaptation at small spatial scales has a significant effect on the success of establishment.
Methods: Reciprocal sowing experiments were carried out among three populations of the species to test for evidence of local adaptation on seedling emergence, survival and size. Studied populations were located at the southernmost margin of the species' range, along the local elevation gradient that leads to a drought stress gradient.
Key Results: Drought stress in summer was the main cause of seedling mortality even though germination mainly occurred immediately after snowmelt to make the best use of soil moisture. The results support the hypothesis that species perform better at the centre of their altitudinal range than at the boundaries. Evidence was also found of local adaptation in seedling survival and growth along the whole gradient.
Conclusions: The local adaptation acting on seedling emergence and survival favours the persistence of remnant populations on the altitudinal and latitudinal margins of mountain species. In a global warming context, such processes may help to counteract the contraction of this species' ranges and the consequent loss of habitat area.
Key words: Silene ciliata, local adaptation, southern border, reciprocal sowing, drought stress, altitude gradient
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Seed germination and seedling survival are probably the most critical stages in the life history of plant populations (Kitajima and Fenner, 2000). Species' distribution, colonization capability and range shifts are, thus, partially determined by limitations on progeny viability (Weltzin and McPherson, 1999, 2000). The centre–periphery hypothesis proposes that conditions for the regeneration of plant populations are less suitable on the boundaries than in the centre of the distribution area (Lawton, 1993; Vucetich and Waite, 2003; Angert and Schemske, 2005). Similarly, in species with a wide altitudinal distribution, a suitability gradient is also found within each mountain range (Körner, 1999). Thus, mountain plants occurring at the lowest altitudinal limits at the species' southernmost margin should face especially harsh constraints on seedling emergence and survival (Hampe and Petit, 2005; Arrieta and Suarez, 2006) mainly due to water shortage (Pigott and Pigott, 1993; García et al., 1999; Castro et al., 2004) and high temperatures (Conolly and Dahl, 1970; Peñuelas and Boada, 2003).
How plants respond to climate warming has recently become of special interest. Recruitment in marginal populations of mountain plants may inform us whether upward and/or poleward shifts take place, or whether local adaptation under unfavourable conditions may play a role in their long-term persistence (Davis and Shaw, 2001; Davis et al., 2005; Jump and Peñuelas, 2005). However, regeneration studies have rarely been conducted at species' lowest altitudinal limits in southern range limits (García et al., 1999; Peñuelas and Boada, 2003; Castro et al., 2004; Hampe, 2005). Alpine habitats are especially useful for evaluating range shifts and local adaptive responses because they provide sharp environmental gradients (Grabherr et al., 1994; Grace et al., 2002; Walther et al., 2005). Mediterranean-type mountains are of additional interest because the water supply is strongly limited (Lavorel et al., 1998; Sanz-Elorza et al., 2003; Michalet, 2006).
Silene ciliata (Caryophyllaceae) is a perennial long-lived plant, inhabiting main mountain ranges in the northern half of the Mediterranean Basin. Its latitudinal range covers a relatively narrow band from 40 to 46°N (Tutin et al., 1995). The species is found from 1200 to 3000 m in northern Spain (Pyrennes and Cantabrian Range), France (Massif Central) and Italy (Appenines), whereas in Central Spain populations occur from approx. 1900 m to the highest peaks (up to 2590 m in Gredos Range) and constitute the species' southernmost margin. This suggests that the lower altitudinal limits of this species are highly limited by physical and biotic environmental conditions and that persistence in the southernmost margin is restricted to isolated refuges at high altitude.
The aim of this study was to assess the main limitations on seedling emergence and performance along an altitudinal gradient, and to evaluate local adaptation at small spatial scales which may favour the persistence of remnant populations at the southern boundary of this species. For this purpose, seedling emergence, survival, growth and cause of death in field sowing experiments were monitored using the reciprocal transplant approach, the most commonly applied method for testing local adaptation (Primack and Kang, 1989). A previous study in this area showed that female reproductive success was very restricted in low-altitude marginal populations, probably due to water shortage (Giménez-Benavides et al., 2006). Similarly, a summer drought was expected to be the main factor constraining progeny viability in populations located at the lowest altitudinal limit.
Specifically, the questions addressed here were as follows. (a) Does water shortage at the low altitude boundary negatively affect progeny viability of S. ciliata, as previously reported for reproductive success? (b) Do S. ciliata populations present different ecotypes that exhibit home site advantage at small spatial scales? (c) What are the main causes of mortality and how do they differ along the altitudinal gradient?
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MATERIALS AND METHODS |
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The species
Silene ciliata Poiret grows in cushions of up to 2 cm in height and 15 cm in diameter. The flowering period begins in late June and lasts about 8 weeks. Flowering stems reach 15 cm in height and bear 1–5 protandrous flowers (Giménez-Benavides et al., 2006). Hand-crossing pollination experiments indicate that S. ciliata is a self-compatible species (Giménez-Benavides, 2006). Mean flower number per plant in the study area ranges from 4·5 to 13·7 across populations, whereas mean fruit set in the studied populations is 0·32 ± 0·34. Fruit capsules contain up to 100 viable seeds of 1·53 ± 0·49 mm in diameter and 0·59 ± 0·06 mg in weight. Mean seed set is 0·24 ± 0·19 (Giménez-Benavides et al., 2006). These capsules open at the top when ripe, and seeds are soon dispersed by stalk vibration.
Seed collection and description of the sowing sites
Three populations were selected along the local altitudinal gradient in Sierra de Guadarrama (Madrid, Spain, 40°N, 3°W). Silene ciliata populations in Sierra de Guadarrama are remnants because they are located at the southernmost margin of the species range, isolated from northern montane populations by large lowland areas (Giménez-Benavides et al., 2006). In each population, seeds were collected directly from 20–25 mother plants from relatively small areas (300–400 m2). The aim of the study was to compare progeny responses at the population level rather than to isolate maternal effects. Therefore, seeds from each population were pooled and thoroughly mixed before sowing to obtain three seed sources. The lowest population was located at 1950 m in the vicinity of Laguna de Peñalara, a lake situated in a late Pleistocene glacial cirque in the timberline zone. Silene ciliata is very rare at this altitude, and occurs in small pasture patches interspersed in a Cytisus oromediterraneus–Juniperus communis sp. alpina shrub matrix with dispersed stunted pines (Pinus sylvestris). The intermediate population was located at 2270 m on the summit of Dos Hermanas 3 km from the low population. This site is covered by grass-dominated communities and C. oromediterraneus–J. communis ssp. alpina shrub formations (Sanz-Elorza et al., 2003). The highest population was located at 2420 m on the summit of Peñalara 2 km from the intermediate population. Summit flat areas and crests are covered by a discontinuous cryophilic pasture dominated by Festuca curvifolia (Escudero et al., 2005). These three localities form the longest altitudinal gradient found in the region (approx. 470 m). Mean annual precipitation is 1350 mm and is concentrated from early October to late May. Average snowcover duration is 100–140 d year–1, usually from November to March (Palacios et al., 2003). Approximately 10 % of the total annual rainfall occurs in the dry summer season (from June to September).
Measurement of environmental variables
Several environmental parameters were monitored during the experiment. Snowmelt date was determined at each site from early survey inspections and digital images of the areas taken at weekly intervals (provided by Dr D. Palacios, Universidad Complutense de Madrid). Air temperature was recorded by portable stations near the sowing sites. Precipitation was recorded only at the intermediate site (40°0'13''N, 3°54'15''W, 2236 m). Volumetric soil water content was measured next to one corner of each sowing plot on every census day during the first growing season (0–6 cm depth, Delta-T HH2 moisture meter, Cambridge, UK). To assess edaphic properties, three soil samples were randomly collected from bare-ground areas (top 10 cm of soil) at each of the three planting sites. Texture (percentage of fine soil, fine gravel and gravel), pH, conductivity, organic matter, nitrogen, phosphorus and potassium content were determined by standard soil analytical procedures following Escudero et al. (2005).
Reciprocal sowing experiments
In 2003, seeds were collected in July–August and stored at room temperature. Seeds were weighed before all experiments. Five sets of ten seeds per population (enough to surpass the level of accuracy of the precision balance, COBOS AX120, d = 0·1 mg) were weighed after being stored for 36 h in a silica-gel drier at room temperature.
Optimal sowing conditions had been previously determined in a preliminary experiment carried out in 2002 (data not shown). Thus, on 11 September 2003 (1–2 months after collection), seeds were sown in their population of origin and in the nearest population in altitude, following the reciprocal scheme presented in Fig. 1. Two simultaneous experiments were carried out: reciprocal sowing between the low and intermediate site (hereafter Experiment 1), and reciprocal sowing between the intermediate and high site (hereafter Experiment2). Two separate experiments were chosen rather than a complete reciprocal experiment among the three sites as the former allowed the detection of differences in progeny viability at small spatial scales. Local adaptation between the extreme sites (low and high margins of the species range) is somehow expected, and is less relevant than the existence of local adaptation processes between closer sites. The local edges were included in the distribution of this plant, but the low and high sites could not be replicated in the area because there were no other populations at these altitudes.
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Seedling emergence (defined as the first census date on which cotyledons were observed above the soil surface) and seedling survival were recorded for 2 years. In 2004, censuses were conducted at 10 d intervals throughout the growing season from 10 May to 10 September. In 2005, censuses were carried out at the beginning and end of the growing season (29 June and 28 September, respectively). In these two censuses, seedling size was determined by leaf number. Each dead seedling was assigned a most likely cause of death. Thus, summer drought was assigned to dried-out seedlings without any visible damage, herbivore/pathogen attack to dead seedlings with external signs of predation such as cotyledon removal, and winter frost to those seedlings that disappeared during winter months or appeared uprooted after snowmelt).
Experimental plots consisted of 16 x 16 cm quadrats randomly distributed in small bare areas at each site. To establish the quadrats, a 5 x 5 grid of 1 cm holes, 3 cm apart, was made on a transparent plastic sheet. This plastic sheet was used for accurate seed placement and subsequent monitoring. Two seeds were sown in each hole to ensure an adequate sample size of seedlings. Seeds were sown individually approx. 3 mm beneath the surface and covered with sieved local topsoil. At each site, four plots were randomly assigned to each seed source. Thus, a total of 1400 seeds were sown. All S. ciliata flowers within a 1 m radius around each plot were removed periodically to avoid contamination by natural seed dispersal. All germinations were recorded and analysed in each survey, but the second seedling to emerge in each hole was removed to avoid inter-seedling competition.
Laboratory germination test
In 2003, a germination test under controlled conditions was simultaneously conducted with a sub-set of the seeds sown in the in situ reciprocal experiment. Seeds were subjected to a cold-wet stratification treatment and incubated at alternating 25/15 °C temperature with a 16 h light/8 h dark photoperiod. These conditions have been shown to be very effective for breaking seed dormancy in S. ciliata (Giménez-Benavides et al., 2005). Seeds from each population were placed between two double layers of filter paper in 8 cm Petri dishes and irrigated with distilled water. Dishes were wrapped in aluminium foil and stored at 4 °C. The length of the stratification period simulated natural conditions. Thus, seeds were placed at 4 °C when the first snowfall occurred at the study area (5 November 2003), and the germination test was initiated at the start of snowmelt (12 May 2004). Another sub-set of the seed batches was stored in plastic vials at 6 °C in darkness until the germination tests were carried out.
In germination tests, four replicates of 25 seeds per population and treatment were placed on two layers of filter paper in 8 cm diameter Petri dishes. Filter papers were kept moistened throughout the germination test (75 d) and every 3–4 d seeds showing radicle emergence were counted and removed. The location of the dishes in the chamber was regularly changed at each census. Tests were carried out in a germination chamber (Selecta Hotcold GL, Barcelona, Spain) equipped with six cool-white fluorescent light tubes (Philips 18 W ‘TL’D standard type, wavelength 400– 650 nm) providing a photosynthetic photon flux density of approx. 19 µmol m–2 s–1.
Data analysis
Differences in soil properties among sowing sites were assessed by means of one-way analyses of variance (ANOVAs). Soil water content was analysed using a repeated-measures ANOVA setting sowing site as between-subject factor and date as within-subject factor. The F statistics for within-subject factor and interaction term were corrected for violation of sphericity assumption (i.e. data collected on adjacent sampling dates are more highly correlated than data from separated sampling dates) (von Ende, 2001).
Differences in seed mass among the seeds of the three sites were analysed using one-way ANOVAs. The effects of population of origin (seed source) and population of sowing (sowing site) on seedling emergence, progeny viability, cause of death and seedling size were modelled by fitting generalized linear models (GLMs) (McCullagh and Nelder, 1989). When the distribution of the response variable was a probability ranging from 0 to 1 (seedling emergence, progeny viability, summer drought mortality), the quasi-likelihood estimation was used instead of the binomial distribution because the data were underdispersed (Venables and Ripley, 1998; Guisan et al., 2002). Poisson estimation, using a ‘log’ link function and setting the variance to ‘mean’, was used when the distribution of the response variable was Poisson like (seedling size). Seed source, sowing site and the interaction term were included as explanatory variables (fixed factors). Regression coefficients were tested for significance by t tests. 
2 tests were also conducted to evaluate whether the selected predictors explained a significant fraction of the deviance (Guisan et al., 2002). Progeny viability (number of established seedlings per seeds sown, sensu Herrera, 2000) was calculated at three intervals: at the end of the first growing season (2004), after the first winter season (2005) and after the second growing season (2005). Statistical analyses were performed using the S-Plus 2000 statistical package (MathSoft, Inc., 1999).
Emergence rate and survival rate were analysed using an accelerated failure-time model (Fox, 2001). This method allows the use of right-censored data (i.e. experiments that end before all seeds germinate, or all seedlings die) to estimate parametric regression models using a maximum likelihood approach. The best failure-time distributions were chosen for the data sets based on the comparison of possible distributions with a likelihood ratio test (Fox, 2001). Thus, a log-logistic distribution was used for the seedling emergence data set and a Weibull distribution for the seedling survival data set. Computations were performed following the SAS LIFEREG procedure (SAS Institute, 1996).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Environmental differences among sowing sites
From 2003 to 2005, the low site was on average 1·8 °C warmer than the intermediate site, and 2·9 °C warmer than the high site. Snowmelt at the low site started 7 d earlier than at the intermediate site, and 18 d earlier than at the high site. Mean temperatures during the growing season (from May to September) averaged 14·4 °C in 2004 and 15·6 °C in 2005. Cumulative precipitation was 323·8 mm in 2004 and 226·8 mm in 2005. July and August of 2005 were especially dry months.
Soil water content differed significantly between sowing sites (F2,25 = 27·32, P < 0·001) and sampling dates (F7,175 = 814·67, P < 0·001 after Greenhouse–Geisser and Huynh–Feldt corrections for departure from sphericity). The high site had the highest soil water content on all sampling dates. The interaction term date x sowing site was also significant (F14,175 = 3·78, P < 0·006 after correction), indicating that soil water content changed at different rates at each site. Soil water content dropped sharply in June, reaching minimum values (<5 %) in late July even at the high site. However, the copious rainfall event in early August 2004 partially mitigated the intense topsoil desiccation during late summer (Fig. 2).
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Soil analyses revealed some differences among sowing sites. Texture significantly differed among altitudes (% gravel, F = 8·56, P = 0·017; % fine gravel, F = 8·79; P = 0·016; % fine earth, F = 7·68, P = 0·022). The high site had the highest gravel content and the lowest fine earth content, while the intermediate site had the highest fine gravel content. A weak acidity gradient was observed from low to high sites (F = 5·15, P = 0·05). No significant differences were found in conductivity and potassium content among sites (F = 2·79, P = 0·139; F = 4·71, P = 0·089, respectively). Organic matter, nitrogen and phosphorus content at the low and high sites were higher than at the intermediate site (F = 57·50, P < 0·001; F = 36·03, P < 0·003; F = 8·79, P < 0·034, respectively).
Seed mass and seedling emergence
Mean seed mass across sites was 0·39 mg. No significant differences in seed mass were found among sites.
In the laboratory germination tests, only 28 % of the seeds germinated after simple storage at 6 °C, but nearly 70 % germinated after the cold-wet stratification treatment, when data from the three seed sources were pooled together. Both seedling emergence (Table 1) and emergence rate (Table 2) significantly improved after cold-wet stratification in all populations. Seed source explained differences in germination rate (seeds from higher sites germinated faster) but not in germination percentage (Table 2).
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Overall seedling emergence averaged 47·7 ± 19·6 % across all sowing sites and seed sources. The germination period began immediately after snowmelt and lasted until mid-June (Fig. 3). Significant differences in seedling emergence were found between sowing sites in both experiments and between seed sources in Experiment 1 (Table 1). Seedling emergence was the highest at the intermediate site and higher in seeds from the intermediate population than in seeds from the low population (Fig. 3). Seed source had a significant but marginal effect on emergence rate in Experiment 1 (Table 2). However, sowing site accounted for an important fraction of the variation found in Experiment 2 (seeds germinated at a slower rate when sown at the higher altitude) (Table 2). As shown in Fig. 3, all seed source populations had a higher germination rate at the intermediate site.
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Progeny viability
Only 10 % of germinated seedlings survived until the end of the experiment. Seedling mortality was highest during the first growing season (77 %), dropping to 9 % the following winter, and then to 4 % the second growing season.
The effect of sowing site on progeny viability was significant and consistent across time in Experiment 1. Thus, seedling survival was higher when sown at the intermediate site (Table 3, Fig. 4). Seed source was non-significant after the first growing season, but this effect could not be analysed thereafter as all seedlings from the intermediate site died the following winter when outplanted. Nevertheless, the significant site x source interaction found in Experiment 1 implies that differences in progeny viability between seed sources did not remain consistent across sowing sites (Table 3). None of the variables in Experiment 2 were significant (data not shown). Seedling survival rate was explained only by sowing site in both experiments (Table 4). Survival curves in Fig. 4 show that mortality slows down after mid-summer precipitations and the subsequent increase in soil moisture (Fig. 2). Analyses of seedling size at the end of the experiment revealed that sowing site had a slight effect in Experiment 1. Thus, seedlings sown at the high site were the largest (Table 5). The effect of the interaction term could not be computed. In Experiment 2, both sowing site and the interaction term were significant. Local seedlings developed more leaves than foreign seedlings at both sowing sites (Fig. 5).
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Summer drought was the most important cause of seedling mortality across sites (86·5 %), followed by winter frost (10·5 %) and herbivore/pathogen attack (3 %). GLMs were conducted to determine whether sowing site and seed source could explain susceptibility to each cause of death. No significant differences were found among sowing sites or seed sources in mortality due to winter frost and herbivore/pathogen attack (data not shown), despite slight trends observed along the altitudinal gradient (Fig. 6). The results of the summer drought mortality model indicated that sowing site (and, to a lesser degree, seed source) partially explained the deaths due to drought in Experiment 1. The low sowing site reached the highest mortality due to drought stress (Table 6, Fig. 6). Neither site nor seed source differed significantly in Experiment 2.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Germination in high mountain areas is mainly restricted to short periods in early summer when temperatures are high enough and soil water from snowmelt is still available (Bliss, 1971). Consequently, seed dormancy, which prevents immediate post-dispersal germination, is a common trait in alpine plant species (Pelton, 1956; Bliss, 1971). It was found that most S. ciliata seeds follow this germination pattern: they required not only a post-dispersal maturation period to germinate, but also a cold-wet stratification for several months (i.e. winter season) (Tables 1 and 2, Fig. 3), as reported for many other alpine species (Marchand and Roach, 1980; Giménez-Benavides et al., 2005; Shimono and Kudo, 2005). After the cold-wet period and snowmelt, germination occurred at a high rate due to adequate soil moisture (Fig. 3). The timing of germination is of critical importance to subsequent seedling survival under seasonal environments (Baskin and Baskin, 1998; Shimono and Kudo, 2003), especially in Mediterranean mountains where soil desiccation is very common during the growing season (Fig. 2).
Results of the reciprocal sowing experiments clearly highlight some local adaptation processes at a small scale favouring offspring success. Although progeny viability was low in both the low and intermediate seed source populations, a significant interaction term was detected at the low site (Table 3). This suggests a certain level of local adaptation as seedling performance was higher for home seeds than for foreign seeds at both sites (Fig. 4).
Several authors have argued that selection for local adaptation is theoretically favoured in rear edge populations, where reduced gene flow due to isolation promotes the existence of distinct ecotypes (Dynessius and Jansson, 2000; Hampe and Petit, 2005; Jakobsson and Dinnetz, 2005). The low S. ciliata population is located on the rear edge, restricted to small open interspaces within a matrix of unsuitable habitat. After the first year, survival of home seedlings at the low site was remarkably higher than that of seedlings from the intermediate source population (>20 percentage points). However, after 2 years, the number of established seedlings was similar and dramatically low irrespective of seed source (Fig. 4). The high mortality caused by the pronounced drought of the second summer, very similar to that recorded during the extreme heatwave of 2003 (Schär et al., 2004), may have overshadowed the initial differences in survival capacity. Other evidence of local adaptation in progeny viability was found in the high seed source population (i.e. on the leading edge of local distribution), which had higher seedling survival in its home site than in the intermediate seed source population (Fig. 4). Despite the fact that such a type of home vs. foreign effects has been interpreted as a consequence of local adaptation (Kawecki and Ebert, 2004), the results should be considered with caution as they could merely reflect differences in home habitat quality. Nevertheless, seedling size, a surrogate of plant performance, also revealed similar local adaptation when seeds from the intermediate and high populations were reciprocally sown (Table 5, Fig. 5B). Moreover, larger seedling size may increase the chance of survival in the following seasons (Shimono and Kudo, 2003).
In spite of the local adaptation effects detected, certain seed sources performed better in all situations, and certain sites were clearly more suitable for species regeneration. A significant seed source effect was found in Experiment 1. Seedling emergence and emergence rate reached higher values in the intermediate seed source population than in the low seed source population regardless of the sowing site (Tables 1 and 2), suggesting a seed quality effect. On the other hand, seedling emergence and progeny viability decreased significantly when seeds from both low and intermediate populations were sown at the low site, suggesting that the low site is the most stressful (Figs 3 and 4). Conversely, the intermediate site, and to a lesser extent the high site, were favourable environments for S. ciliata regeneration. Soil analyses showed that the low site has the largest amount of fine earth fraction and higher organic matter, nitrogen and phosphorus content than the intermediate site, all surrogates of soil development. This suggests that site suitability for germination and seedling survival is not determined by these edaphic properties. In contrast, lower soil water content and higher temperature seem to be the main limitations for seedling establishment at the low site. In fact, it was recently found that reproductive success of the low population was extremely low, especially in dry years, when many mature plants were simply unable to flower. In contrast, the intermediate and high populations provided higher and more stable seed production over time (Giménez-Benavides et al., 2006). Thus, the results support the centre–periphery hypothesis that performance is better at their range centre than at the margins, and that severe abiotic limitations constrain the lowland boundary (Lawton, 1993; Hampe and Petit, 2005).
It is important to note the great impact of summer drought on progeny viability. The low site had significantly higher mortality due to water shortage than the other sites (Table 6, Fig. 6), supporting the initial assumption and previous findings on S. ciliata reproductive output (Giménez-Benavides, 2006). Since the sowing experiments were carried out in bare soil patches, the major cause of seedling mortality during the growing season can be reliably assigned to drought stress rather than to competition. High levels of drought-induced mortality are a common feature from lowland to mountainous habitats in Mediterranean-type ecosystems (Dunne and Parker, 1999; Escudero et al., 1999; Castro et al., 2004, 2005). However, it has rarely been experimentally documented in high mountain Mediterranean-type environments (see Cavieres et al., 2005 regarding Mediterranean-type mountains in Central Chile). The results support the recent hypothesis that water shortage is a key factor controlling plant performance in high Mediterranean mountains (Cavieres et al., 2006; Michalet, 2006). Mountain habitats have been considered extremely stressful for plant life but normally not limited by water availability (Körner, 1999). However, Mediterranean mountain specialists cope with both a very short growth season, typical of all mountain environments, and a severe water shortage in summer. Silene ciliata populations in Central Spain are a clear example of remnant populations within the plant distribution area, a factor commonly associated with regression dynamics due to climatic stress (Eriksson, 1996; García et al., 1999; Hampe and Petit, 2005). An increasing number of studies are reporting the prevalence of facilitative interactions that partially counteract the effects of stressful conditions in Mediterranean mountains (Castro et al., 2004; Cavieres et al., 2005, 2006; Gómez-Aparicio et al., 2005a, b), but the potential role of species' local adaptation in offspring establishment success has not been explicitly explored.
On the other hand, studies on local adaptation in populations located on an elevation gradient are very scarce (Clausen et al., 1940; Galen et al., 1991; Etterson, 2004; Angert and Schemske, 2005). Surprisingly, these studies have commonly used juvenile or adult plants as a starting point in reciprocal transplant experiments instead of seeds (but see Shimono and Kudo, 2003). The lack of evidence of local adaptation found in some of these studies may have resulted from the use of reciprocal transplants instead of sowing experiments (Clausen et al., 1940; Galen et al., 1991). Such approaches do not properly explore the role of natural selection in critical earlier life history stages (Primack and Kang, 1989; Angert and Schemske, 2005). Although seedling establishment has been predicted to be rare in alpine habitats because of dominant life history trade-offs, recent evidence suggests that habitat selection in early life history stages in mountainous habitats must not be undervalued (Chambers, 1995; Forbis, 2003; Shimono and Kudo, 2003; Castro et al., 2004).
In conclusion, the local adaptation acting upon seedling emergence and seedling survival and growth in S. ciliata may help partially to counteract environmental limitations, allowing the local persistence of peripheral populations. Understanding the limitations on recruitment in plant populations at the extreme margin of their species' distributions may provide valuable information on plant response plasticity and evolutionary potential to cope with rapid climate warming (Jump and Peñuelas, 2005). Nevertheless, population dynamics and range shift processes cannot be properly estimated through simple recruitment rates, at least for long-lived species such as S. ciliata (García et al., 1999; García and Zamora, 2003; Hampe and Petit, 2005). Long-term demographic monitoring, in conjunction with the assessment of genetic patterns and ecosystem processes operating at various spatiotemporal scales, are needed to integrate current knowledge of climate change impacts across the species' ranges.
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ACKNOWLEDGEMENTS |
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We thank the staff of Parque Natural de las Cumbres, Circo y Lagunas de Peñalara for permission to work in the area, and C. Iriarte, B. Martínez, Y. Valiñani and B. Paredes for the analyses of soil samples. We also thank T. Forbis and M. J. Albert for helpful comments on earlier drafts of the manuscript, and L. De Hond for her linguistc assistance. This work was supported by the Spanish Government CICYT project REN2003-03366.
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LITERATURE CITED |
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