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Ann Bot. Nov 2007; 100(6): 1189–1197.
Published online Sep 26, 2007. doi:  10.1093/aob/mcm214
PMCID: PMC2759255

Ecology of Achene Dimorphism in Leontodon saxatilis

Abstract

Backround and Aims

Leontodon saxatilis produces two morphologically distinct achenes (morphs) in a single capitulum: one row of dark brown achenes without a pappus lies at the edge (‘peripheral achenes’; 0·74 ± 0·18 mg) while the inner ones are light brown with a pappus (‘central achenes’; 0·38 ± 0·07 mg). The hypothesis that achene heteromorphism in L. saxatilis widens its ecological amplitude was tested.

Key Results

Achenes of both morphs germinated over the same range of temperatures (6–33 °C) but the central achenes showed significantly higher germination percentages, and the two also differed significantly in their annual dormancy cycle, with the peripheral achenes showing greater dormancy for part of the year. Seedlings from the two morphs did not differ significantly in total biomass after 2 and 4 weeks of growth, neither did they differ significantly in root and shoot weight and root:shoot ratio. Plants from both morphs growing at different regimes of soil moisture, nutrients and competition did not differ significantly in their number of achenes per capitulum. While the number of central achenes varied, that of peripheral achenes remained constant at approx. 13. Drier soil led to an increase in the number of central achenes in plants from both morphs.

Conclusions

The peripheral achenes can replace the mother plant in the following growing season, whereas the central achenes are well adapted for wind dispersal and thus for colonization of new sites. However, the extent of variation in germination characteristics was similar to that found in seed populations of homomorphic plants, which suggests that germination percentage and other growth characteristics do not contribute to widening the ecological amplitude. The habitat of most heteromorphic species, the morphs of which differ greatly in germination and/or growth characteristic, are deserts or highly disturbed areas where such differences are highly advantageous, but in the moderate habitat of L. saxatilis the differences may prove a disadvantage.

Key words: Achene morphology, Asteraceae, dormancy cycle, germination, Leontodon saxatilis, seed heteromorphism, seedling growth

INTRODUCTION

Reproduction from seeds, i.e. germination and establishment, is a bottleneck in many plant species and determines the ecological amplitude and therefore the distribution of species (Olff et al., 1994, Grime, 2001). Compared with vegetative reproduction, reproduction from seeds involves a higher risk of mortality because seedlings are much more vulnerable to such unfavourable environmental conditions as frost, shade, and drought (Harper, 1977). Therefore, the ‘right’ time for germination in a favourable habitat is decisive not only for the survival of seedlings (Thompson, 1973) but also for successful establishment of a species and long-term maintenance of its population. For this reason, seed properties, especially morphology, that affect dispersal, dormancy and germination can confer a high selective advantage (Meyer et al., 1990; Schütz and Milberg, 1997). The morphology of a seed is closely related to a number of potentially conflicting requirements (Thompson et al., 2002), which are reflected in such trade-offs as seed number vs. seed mass or seed mass vs. dispersal ability. Seed morphology (e.g. pappus and wings) and mass are decisive for anemochorous dispersal (Meyer and Carlson, 2001; Thompson et al., 2002) and determines, among other things, soil seed bank (Rees, 1993, 1996; Eriksson and Eriksson, 1997), dormancy (Leishman et al., 2000) and germination characteristics (Pons, 1991). Moreover, seedling emergence (Jurado and Westoby, 1992; Leishman et al., 2000; Jensen and Gutekunst, 2003; Eckstein and Donath, 2005) and survival rates differ between those from large and small seeds (Jurado and Westoby, 1992; Bosy and Reader, 1995; Turnbull et al., 1999). Consequently, since relatively small differences in seed morphology may lead to large differences in germination, seedling emergence and viability, most plant species show only slight intraspecific differences in seed morphology and/or seed mass (Harper, 1977; Gibson, 2001). However, in the course of evolution, some plant species (for an overview, see Imbert, 2002) have developed the ability to produce two or more morphologically different seeds (the so-called morphs) on a single individual plant or even within one inflorescence. These differences can be related to mass (McEvoy, 1984), shape (Williams and Harper, 1965), colour (Marks and Akosim, 1984) and structures for dispersal (Imbert et al., 1997). In some species, the morphs have been found to differ in dispersal (Baker and O'Dowd, 1982; Mandák and Pyšek, 2001a), ability to persist in a seed bank (Mandák and Pyšek, 2001b), germination characteristics (Porras and Munoz, 2000; Brändel, 2004), growth rate of seedlings (Sorensen, 1978) and seedling survival (Forsyth and Brown, 1982). Heteromorphic seeds may enable these species to enhance their spectrum of safe-sites for germination and to establish under a wider range of environmental conditions (Harper, 1977; Flint and Palmblad, 1978).

Studies on Atriplex sagittata (Mandák and Pyšek, 1999a,b, 2001a,b, 2005) and Galinsoga parviflora (Rai and Tripathis, 1987) have so far been confined to examining the consequences of seed heteromorphism on life cycles of the plants, and a widening of ecological amplitude has been predicted as a consequence of seed heteromorphism. Rai and Tripathis (1987) suggest that seed heteromorphism may increase the invasive power of Galinsoga parviflora.

Leontodon saxatilis (Asteraceae) also produces heteromorphic achenes (see below), a fact which has not been considered in most studies so far (Grimoldi et al., 1999; Edwards et al., 2001a,b). The present study sought to investigate whether differences between the two morphs of L. saxatilis with regard to dormancy, germination characteristics, and seedling growth, and morph production itself, confer any advantage in terms of survival of populations and establishment. To this end, the following were determined: (a) the morphology (mass/embryo mass, shape, colour) of achenes within a capitulum; (b) the spectrum of constant temperatures suitable for germination, the annual course of dormancy (dormancy cycle); and characteristics of seed bank (transient, short-term persistent); (c) biomass and root:shoot ratio of seedlings; (d) the proportions of the morphs within one capitulum in plants raised from different morphs; and (e) the response of plants (expressed in terms of the number and proportion of morphs within a capitulum) raised from different morphs to different growth conditions (nutrient and water supply, density/competition).

MATERIALS AND METHODS

Study species and achene collection

Leontodon saxatilis Lam., a sub-Atlantic-Mediterranean species distributed all over Europe and North-west Africa and a neophyte in North America and Australia (Hegi, 1954; Edwards et al., 2001a,b), grows in grasslands of low productivity, fens, and dikes on mesic, partly inundated loamy soils and also in heathlands and sand-dunes on sandy soils. The species is a self-incompatible and annual to biennial member of Asteraceae (Liguliflorea) and flowers between July and September.

In September 2004, achenes were collected from populations at three locations in Schleswig-Holstein (northern Germany): near Eiderstedt (54°25N, 8°56E), near Molfsee (54°16N, 10°4E), and near Sankt Peter-Ording (54°18N, 8°38E). One capitulum was removed from about 100 from Eiderstedt and about 50 each from the other two locations. Achenes from the capitula were air-dried after collection and stored dry at room temperature (15–20 °C, 40–60 % RH) in paper bags until use (which was 12 weeks for expts 1 and 2, 5 months for expt 3, and 10 months for expt 4). The different morphs (see below) were sorted by hand under a stereo-microscope. All experiments except expt 1 were conducted only with achenes from the population from Eiderstedt.

Experiment 1: range of temperatures for germination

The experiment on effect of temperature was carried out in a thermogradient incubator (Rubarth Apparatebau, Hannover, Germany; for details, see Ekstam and Bengtsson, 1993) equipped with warm fluorescent light (Philips TL 20 W/29 RS) providing a photosynthetic photon fluence rate of 75 µmol m−2 s−1 and a Pr/Pfr ratio of about 14·5. Three replicates of 30 achenes each for each temperature regime in one of the chambers of the incubator were used for both the morphs. To determine the range of temperatures suitable for germination of dry-stored achenes, the achenes were kept at 13 different constant temperatures (from 3 °C to 39 °C at 3° intervals). The experiment was carried out in light (12 h d−1). The achenes were examined daily for germination during a 2-week period to calculate the rate of germination. Achenes from the populations of Sankt Peter-Ording and Molfsee were tested only at nine temperatures (from 9 °C to 33 °C) and controlled only twice for germination, once a week after sowing and then 1 week later, at the end of the experiment.

Protrusion of the radicle was the criterion of germination in the experiments. After the experiments, the non-germinated achenes were pinched with forceps to see if the embryos were white and firm, an indication that the embryos were alive; if not, they were considered dead and excluded from the calculations of germination percentages (Baskin and Baskin, 2001).

Experiment 2: burial experiment

In December 2004, fine-mesh nylon bags filled with the achenes were buried – one bag of each morph to one pot – in plastic pots 5 cm deep and 9 cm in diameter with drainage holes at the bottom and filled with a mixture of 75 % loam and 25 % sand. Each bag contained approx. 160 achenes and 52 bags for each of the two morphs. The pots were buried up to the rim along the edge of a canopy of deciduous shrubs and trees in the experimental garden of the University of Hamburg.

The buried achenes were retrieved monthly, starting in March 2005 (when they had been buried for 3 months) and ending in March 2006. On each date, three pots each representing one replicate, were exhumed and transferred to the laboratory. In the laboratory, the bags were removed from the pots under dimmed filtered light (‘bright blue’ and ‘light red’ filters; LEE-filter, Andover, UK) to avoid wavelengths that influence germination. Achenes from each bag were distributed among 4 Petri dishes lined with filter paper (Filtrak Type 10; Munktell&Filtrak GmbH, Bärenstein, Germany) moistened with deionized water and incubated at 20 °C/10 °C (10 h each temperature and 2 h of warming and cooling, respectively) and at 20 °C under light (12 h d−1) and darkness in incubators (Rubarth Apparatebau, Hannover, Germany) equipped with warm fluorescent light (Philips TL 20 W/29 RS) providing a photosynthetic photon fluence rate of approx. 100 µmol m−2 s−1 and a Pr/Pfr ratio of 6·5.

The achenes were examined weekly for germination until the end of the experiment after 4 weeks.

Experiment 3: seedling growth

To study seedling growth, achenes of both morphs were germinated in an incubator (see above) at 20 °C/10 °C in light (12 h d−1) in Petri dishes on moistened filter paper. After 4 d, 28 germinated achenes for each morph were transferred to the greenhouse (20–25 °C) and sown in 5-cm-deep plastic pots filled with fine sand. Half the seedlings were given only deionized water while the other half were given a nutrient solution (0·9 g L−1 total-N, 0·5 g L−1 P, 1·1 g L−1 K and trace elements). After 2 and 4 weeks of growth, seven seedling of each morph were harvested from both the treatments and their fresh and dry masses were recorded, separately for roots and shoots.

Experiment 4: environmental influence on morph production

The experiment on the effect of the environment was split in two subsets. Soil water content and density/competition were manipulated in the first subset and nutrient supply in the second.

For the first subset, achenes of both morphs and achenes of Hypochoeris radicata were germinated in Petri dishes on moistened filter paper in incubators (see above). Hypochoeris radicata was chosen because it has the same growth form (a rosette) and has shown similar reactions to different growth conditions (Edwards et al., 2001a, b). When seedlings had produced their first leaf, they were transplanted to 12-cm-deep plastic pots filled with loamy soil (Einheitserde 0, Einheitserdewerk Uetersen; Werner Tantau GmbH & Co. KG, Germany) supplemented with 3 g L−1 soil of Plantosan (20 % total N, 10 % P2O5, 15 % K2O, 6 % MgO and trace elements; Spiess-Urania Chemicals GmbH, Hamburg, Germany). A factorial design was adopted with two kinds of plants (raised from the two morphs, namely the central and the peripheral achenes), two moisture levels (soil held at field capacity all the time and soil dried out irregularly), and three competition/density levels: (1) one plant of L. saxatilis per pot (the so-called target plant); (2) one target plant in the middle of the pot surrounded by three more of the same species; and (3) one target plant surrounded by three plants of H. radicata. The plants were grown in the greenhouse with windows open throughout the year.

For the second subset, plants of each morph were grown separately in 12-cm-deep plastic pots filled with loamy soil (Einheitserde 0, see above) supplemented with either a lower dose of nutrients [1 g Plantosan (see above) L−1 soil] or a higher dose (6 g Plantosan L−1 soil), in the botanical garden of Hamburg.

All the test regimes were replicated ten times. When achenes of the target plant were ripe, five replicates of each regime were chosen randomly and five heads were harvested from each target plant. The peripheral and central achenes were counted separately for each capitulum. For plants where the nutrient supply had been varied, the number of capitula per plant was counted after the growing season, when the plants were dead.

Statistical analysis

Germination data were analysed by Logistic Regression models using SAS-procedure Logistic (SAS, 1996); see Hosmer and Lemeshow (2000). Over-dispersion was corrected with the Williams method (SAS, 1996). In expt 1, four separate models were calculated. The first model comprised three factors, namely the morph (central and peripheral), test temperature (eight out of the 13 test temperatures) and provenance (Eiderstedt, Molfsee and Sankt Peter-Ording) and all interactions. The test temperatures at which any morph failed to germinate were excluded from the model (3 °C and 6 °C and 33 °C, 36 °C, and 39 °C). The other three models comprised two factors, namely morph and temperature, and their interactions were tested separately for each of the three populations. Later, the morphs at the different test temperatures were compared in pairs for each population using the contrast statement within the logistic regression model. The model for the burial experiment (expt 2) comprised two factors, namely morph (central and peripheral) and the date on which the pots were retrieved (13 dates representing the monthly intervals).

Differences between morphs in achene mass, distribution of mass within achenes and in days to 50 germination (t50) (expt 1) as well as differences in fresh and dry weight and root : shoot ratio (expt 3) in the seedlings were analysed by Welch two sample t-tests (R, version 2·4·1; http://cran.r-project.org).

For differences between morphs and treatment effects on the production of morphs within one capitulum (expt 4), the data were analysed by ANOVAs using R (Version 2·4·1; http://cran.r-project.org). The achene number per capitulum of one target plant was analysed for normality and homogeneity of variances. As both criteria were fulfilled in nearly all plants, the mean value of central and peripheral achenes per capitulum of the five capitula for each plant were included in the ANOVA to avoid pseudoreplication (Crawley, 2005). All data were tested for normality and homogeneity of variances prior to the analysis to fulfil requirements of ANOVA and t-tests.

RESULTS

Morphology of achenes

Within a capitulum, most achenes are light brown, slightly beaked to straight and elongated, with a pappus with two rows of hair (the central achenes; Fig. 1). At the edge of the capitulum lies one row of the peripheral achenes, which are larger and darker and have only a small ring of hair instead of a pappus (Fig. 1). Total achene mass as well as embryo and pericarp mass of the peripheral achenes was significantly higher than that of the central achenes (Fig. 2; data only for the population Eiderstedt, total: d.f. = 50·9, t = 12·5, P < 0·001; embryo: d.f. = 65·6, t = 8·3, P < 0·001; pericarp: d.f. = 44·4, t = 13·7, P < 0·001). However, in the central achenes a significantly higher proportion of total mass was allocated to the embryo (60 ± 0·2 %), compared with 46 ± 0·2 % in the peripheral achenes (d.f. = 76·3, t = −10·8, P < 0·001). Pericarp in the peripheral achenes was more than twice as thick as that in the central achenes (Fig. 3) and contained many more sclerenchymatous cells.

Fig. 1.
Peripheral (left and middle) and central (right) achenes of Leontodon saxatilis.
Fig. 2.
Mean weight (± s.e.) of embryo and pericarp of central and peripheral achenes of Leontodon saxatilis.
Fig. 3.
Cross-section of the pericarp of central (left) and peripheral (right) achenes of Leontodon saxatilis.

Experiment 1

After 12 weeks of dry storage, achenes of both morphs (collected from Eiderstedt) germinated (germination greater than 5 %) when maintained at temperatures between 6 °C and 30 °C (Fig. 4A). However, the optimal range (>80 %) was between 9 °C and 27 °C for the central achenes and between 12 °C and 21 °C for the peripheral achenes. Over the whole temperature range, germination percentage was significantly higher in the central achenes (Fig. 4A). The number of days to reach 50 % of the final germination percentage (t50) was only slightly different at temperatures ≤21 °C but at higher temperatures, the central achenes showed lower values of t50 (Table 1). However, because of the large variation, values of t50 differed significantly between the two morphs only at 27 °C (d.f. = 4, t = −4·9, P < 0·01).

Fig. 4.
Final germination percentages (± s.e.) of central and peripheral achenes of Leontodon saxatilis at a range of constant temperatures. Seeds of three populations, namely those from Eiderstedt, Molfsee and Sankt Peter-Ording were tested. Light was ...
Table 1.
Days to 50 % germination (t50) for peripheral and central achenes as influenced by temperature during the 14-d test period (means ± s.e.)

All the three populations showed similar germination patterns of the two morphs at the temperatures tested (Fig. 4). The logistic regression model showed that germination of the two morphs at the different test temperatures did not differ significantly among the three populations (morph × temperature × population: d.f. = 14, Wald chi-square = 20·3, P = 0·12). In both, the Eiderstedt and Molfsee population logistic regression models showed a significant ‘morph’ * ‘temperature’ interaction indicating that differences in germination percentages between morphs varied among test temperatures (Eiderstedt: d.f. = 7, Wald Chi-Square = 30.4, P < 0.001; Molfsee d.f. = 7, Wald Chi-Square = 25.7, P < 0.001). On the other hand, the two morphs from the population at Sankt Peter-Ording did not differ significantly in germination percentages at the optimal range, namely between 15 °C and 24 °C (Fig. 4C).

Experiment 2

At the beginning of the experiment, dry-stored achenes of both morphs germinated in light to nearly 100 %. There were only slight differences in germination at 20 °C/10 °C in darkness, but at 20 °C in darkness, germination was 85 % in the central achenes and only 20 % in the peripheral achenes.

Achenes of both morphs showed an annual dormancy cycle with high germination during winter (December to March) and lower germination from April to November (Fig. 5B–D). Although at 20 °C/10 °C in light and in darkness, germination percentages were similar during the test period in achenes of both morphs, the percentages fluctuated greatly in the peripheral achenes in darkness and sometimes reached low values. The logistic regression model showed no significant differences in the course of dormancy during the test period when achenes were tested at 20/10 °C (light: morph × date of retrieval d.f. = 12, Wald chi-square = 8·9, P = 0·72; darkness: morph × date of retrieval d.f. = 12, Wald chi-square = 13·3, P = 0·35).

Fig. 5.
Final germination percentages of central and peripheral achenes of Leontodon saxatilis incubated under light and in the dark at 20 °C and 20 °C/10 °C following 0–24 months of being buried in an experimental garden. Bars ...

At 20 °C in light, germination percentages of both morphs showed large differences: in late summer, the figure dropped to 25 % in the peripheral achenes but was 70 % in the central achenes. In darkness, the peripheral achenes reached maximum germination in winter 2004/05 not before mid-April while the central achenes already showed an induction of dormancy at the same time. The logistic regression model showed that the course of dormancy during the test period was significantly different between the two morphs at 20 °C (light: morph × date of retrieval d.f. = 12, Wald chi-square = 21·54, P < 0·05; darkness: morph × date of retrieval d.f. = 12, Wald chi-square = 48·96, P < 0·001)

Experiment 3

Fresh and dry mass of seedlings growing out of the two morphs did not differ significantly (P > 0·05) either after 2 weeks or after 4 weeks of growth (Fig. 6, dry weight data not shown). There were no significant differences (P > 0·05) in root and shoot mass and in root:shoot ratio in seedlings of the two morphs. After 2 weeks of growth, root : shoot ratio in both morphs was nearly 1 in seedlings that had received only deionized water whereas it was 5 in seedlings that had received the nutrient solution. By 4 weeks of growth, the ratio showed a greater proportion of shoot in all seedlings: it had declined to 0·5 (deionized water) and 1·5 (nutrient solution).

Fig. 6.
Fresh weight (mg ± s.e.) of Leontodon saxatilis seedlings raised from central and peripheral achenes. Seedlings were harvested after 2 and 4 weeks.

Experiment 4

Both the subsets (differing moisture levels and different degrees of density/competition water on one hand and different doses of nutrients on the other) resulted in variation in the number of achenes in a capitulum, which ranged between 86 and 114 in the first subset (Table 2) and between 68 and 81 in the second (Fig. 7). At the same time, the number of peripheral achenes was almost constant (12 or 13) in nearly all the harvested capitula – it was only the number of central achenes that accounted for the variation due to the different treatments.

Fig. 7.
Total number of achenes per capitulum (± s.e.) of Leontodon saxatilis plants grown from peripheral and central seeds. Plants were grown with greater (+) and smaller (–) supply of nutrients.
Table 2.
Total number of achenes per capitulum of plants grown from central and peripheral achenes under growing conditions that differed in competition, density and water supply

Plants of the two morphs grown at different levels of soil moisture and density/competition did not differ in their total achene production, as revealed by the non-significant factor morph (d.f. = 1, F = 0·31, P = 0·58) and the non-significant interactions morph × water (d.f. = 1, F = 0·26, P = 0·62), morph × competition (d.f. = 2, F = 1·57, P = 0·21), and morph × water × competition (d.f. = 2, F = 2·03, P = 0·14). However, production of central achenes was affected by the level of soil moisture. Drying out of the soil from time to time led to a significantly higher number of central achenes than was seen in plants grown in soil with water always at field capacity (d.f. = 1, F = 9·27, P < 0·01). The non-significant interaction water × competition showed that water exercised its effect independent of the degree of competition and planting density.

As regards differences in nutrient supply, the factors morph and fertilizer had no significant effect (P > 0·05) on achene production. However, when supplied with greater quantities of nutrients, plants raised from central achenes produced significantly more central achenes than those raised from peripheral achenes (morph × fertilizer: d.f. = 1, F = 5·69, P < 0·05).

The number of capitula per plant did not differ between plants of either morphs growing under a lower supply of nutrients and was approx. 33. At higher levels of nutrients, plants raised from peripheral achenes produced slightly more capitula (69 ± 14) than those raised from central achenes (55 ± 13) but this difference was not significant (P > 0·05).

DISCUSSION

In some members of Asteraceae that exhibit heteromorphism of achenes, the achenes differ more or less continuously from the centre to the periphery of the capitulum, e.g. Bidens odorata (Corkidi et al., 1991); in others, e.g. Picris echioides (Sorensen, 1978), the change in seed morphology is abrupt, as is the case in L. saxatilis. It is noteworthy that production of peripheral achenes in L. saxatilis is restricted to the outer ring of florets that are morphologically equal to the central florets (hermaphrodite ray flowers).

The most obvious difference between morphs of L. saxatilis lies in their dispersal ability, due largely to the pappus, which is present only in the central achenes (terminal velocity 0·97 m s−1; M. Kleyer et al., unpubl. res.; Oldenburg, Germany.). However, peripheral achenes are often attached to the bracteens (personal observation), which might also help in hydrochory (Kigel, 1992) and epizoochory (Sorensen, 1978). Apart from seed dimensions, it is the seed mass that is decisive in dispersal (Meyer and Carlson, 2001), an observation that reinforces the better dispersal ability of the lighter central achenes. This pattern is found in the majority of heteromorphic members of Asteraceae (McEvoy, 1984; Rai and Tripathis, 1987).

The peripheral achenes in L. saxatilis, on the other hand, have a thicker pericarp with more sclerenchymatic cells, which may protect the seed from soil biota and mechanical damage. However, after 2 years of being buried the two morphs showed no difference in the proportion of viable achenes; thus, both morphs can build up, at least, a short-term persistent seed bank (cf. Thompson et al., 1997).

Venable et al. (1987) describe the so-called low-risk/high-risk strategy in heteromorphic species: the lighter morphs, better adapted for dispersal, show a higher germination rate and higher germination percentages than the heavier morphs, which are less suited to dispersal. Consequently, one kind may colonize new sites whereas the other remains in the vicinity of the mother plant (Venable et al., 1987). The present results show very clearly that morphs of L. saxatilis follow this strategy. It was also shown for the first time that seed morphs of a species differ in their annual dormancy cycle. Following the low-risk/high-risk strategy, the peripheral achenes show a higher degree of dormancy during part of the year. Nevertheless, seeds of both morphs exposed to light and fluctuating temperatures are able to germinate to high percentages at any time of the year. So far, there have only been some indications that seed morphs can differ in their degree of dormancy (Venable et al., 1987). However, in many heteromorphic members of Asteraceae the lighter central achenes show significantly higher germination percentages and/or faster germination and/or a wider tolerance to germination conditions than the peripheral achenes (Forsyth and Brown, 1982; McEvoy, 1984; Imbert et al., 1996). In some of these species and even in the closely related Leontodon longirrostris such differences are much more pronounced (Hensen, 1999; Ruiz de Clavijo, 2001) than those in L. saxatilis. To produce seeds that differ greatly in germination characteristics and in seedlings they grow into is an adaptation to frequently disturbed and extreme habitats (e.g. deserts) because it may enhance the probability of survival of such populations or even of the species. The most pronounced differences in morphs are found in species that occur in such habitats (Kigel, 1992; Porras and Munoz, 2000; Gibson, 2001; for a list of heteromorphic species, see Imbert, 2002). But in species that occur in more stable and milder habitats, variable germination may be a disadvantage because a short, specified season or a distinct set of environmental condition is suitable for germination and seedling establishment and the two must take place during that season or under these conditions. This may be the reason why only small differences in germination characteristics are found in heteromorphic species of more or less moderate habitats (e.g. Baker and O'Dowd, 1982). The differences between the closely related L. longirrostirs, which occurs in a more extreme habitat in the Mediterranean (Hensen, 1999; Ruiz de Clavijo, 2001) and L. saxatilis populations, which occur in northern Germany, are a good example that supports this hypothesis. Thus, production of heteromorphic seeds does not necessarily lead to greater differences in germination characteristics (see also Marks and Akosim, 1984; Smith and Cawling, 2002). Differences in germination requirements of the seed populations of L. saxatilis seem to be not much greater than those found in homomorphic species (e.g. Bouwmeester and Karssen, 1992, Schütz, 1997). Leontodon saxatilis achenes of both morphs germinated mainly in autumn after shedding but also in the next spring (data not shown).

In general, species with larger seeds produce larger seedlings and have higher recruitment success (e.g. Jakobsson and Eriksson, 2000) but also have lower seedling growth rates (Gleeson and Tilman, 1994). In contrast, seedlings produced by the two morphs in L. saxatilis showed no significant differences in seedling weight, a pattern also found in some other heteromorphic species (e.g. Venable and Levin, 1985). For seedling growth, seed reserve mass is more decisive than total seed mass as it best reflects the seedling's resources (Leishman et al., 2000). In Asteraceae, such reserves are stored in the embryo (Fenner, 1983). This seems to be the main reason why differences in seedling growth between morphs were not as high as may be expected from the differences in total achene mass, at least in L. saxatilis. It is therefore concluded that differences in achene morphology had no effect on seedlings growth characteristics in L. saxatilis. Given these results, the morphs are unlikely to exhibit differences in growth characteristics of adult plants as found by some researchers, e.g. Imbert et al. (1997) in Crepis sancta.

The conditions under which the mother plant grows influence many characteristics of its seed (Gutterman, 1981, 2000; Roach and Wulff, 1987). In some species with heteromorphic seeds, for example, the proportion of morphs in the inflorescence changes in response to environmental conditions (Maurya and Ambasht, 1973; Baker and O'Dowd, 1982). It may be an adaptive response to unfavourable conditions to produce in greater proportion those morphs that have better dispersal abilities to ‘escape’ the unfavourable conditions and, under favourable conditions, switch to greater proportions of morphs that are poor in dispersal abilities but more suited to the habitat to maintain a presence in the favourable habitat. A striking point of the present study is that L. saxatilis increases the number of central achenes when water is in short supply. Although the total number of achenes did not vary with different levels of nutrient supplies, it is possible that differences between the levels of nutrient supply were too slight to elicit a different response. Heteromorphic species have not been found to be consistent in adopting this strategy of producing a higher proportion of morphs with better dispersal abilities as a response to unfavourable conditions (Baker and O'Dowd, 1982; Ruiz de Clavijo, 1995; Mandák and Pyšek, 1999a, b; Imbert and Ronce, 2001). However, it is remarkable that the number of peripheral achenes in L. saxatilis remains constant despite changes in nutrient supply, water availability, and density/competition, a constancy which suggests a genetically fixed attribute – what varies is the number of central achenes, which are better suited for dispersal.

Although differences in plants raised from different morphs have rarely been studied, larger seeds are known to produce larger plants with greater reproductive output (Weiss, 1980; Cheplick and Quinn, 1982; Ellison, 1987; Imbert et al., 1996). Under higher nutrient supply, the peripheral achenes of L. saxatilis produced plants that, in turn, produced slightly more capitula per plant; under the same conditions, the central achenes produced plants with a significantly greater number of achenes per capitulum. Thus, no clear difference emerged between the reproductive outputs of either kind of morph.

These results show that the effects of seed heteromorphism in L. saxatilis are similar to those in most other heteromorphic species that have been investigated, namely (a) better adaptation for dispersal, (b) higher germination percentages and germination rate of central achenes, and (c) the ability to change the proportion of morphs within a capitulum under different environmental conditions. However, the kind and the extent of differences caused by seed heteromorphism in L. saxatilis populations form northern Germany make it difficult to assess whether such a response can widen ecological amplitude or enhance invasive power. Further studies are necessary to clarify whether populations from other more extreme habitats or regions exhibit any differences between morphs or the absence of differences is a general feature of this species. Differences between the two morphs in their dispersal ability are obviously of great ecological relevance to the annual to biannual species because such differences reduce the risk of local extinction due to local events in all populations.

ACKNOWLEDGEMENTS

I thank Lutz Eckstein, Kai Jensen for comments of earlier drafts of the manuscript, Detlef Böhm, Anke Brandt, Sandra Burmeier, Karen Harder, Marion Klötzel, Jutta Krüger, Claudia Mählmann and Tanja Nack for their assistance in the experiments, the botanical garden for area for the growth and burial experiments and the DFG for funding (BR 2896/2–1).

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