Annals of Botany 90: 279-286, 2002
© 2002 Annals of Botany Company
Role of Within-individual Variation in Capitulum Size and Achene Mass in the Adaptation of the Annual Centaurea eriophora to Varying Water Supply in a Mediterranean Environment
1 Departamento de Biología Vegetal, Facultad de Ciencias, Universidad de Córdoba, Colonia San José 4, Campus de Rabanales, E-14071 Córdoba, Spain
* For correspondence. Fax 957218598, e-mail bv1rucle{at}uco.es
Received: 21 January 2002; Returned for revision: 13 March 2002; Accepted: 17 May 2002
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ABSTRACT |
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To clarify the adaptive value of variation in capitulum size and achene mass, plants of Centaurea eriophora were studied in a glasshouse and in a natural population. C. eriophora plants consist of a basal leaf rosette from which an erect stem grows, with lateral branches of various orders ending in capitula of different orders. Primary, secondary and tertiary capitula are comparable in size and they produce similar numbers of achenes, which are similar in weight (large achenes). These capitula are formed during April, May and early June, and constitute the normal or primary flowering. Following ripening of tertiary capitula, leaves senesce, but, later during June and the first half of July, a secondary flowering of a variable number of smaller capitula may occur if wet conditions persist for longer than usual. Plants that have almost senesced develop small lateral branches 1–2 cm long bearing a few small leaves and ending in a capitulum about half the diameter of capitula from the primary flowering period. The number of achenes produced in these capitula (small achenes) and their weight are 70 and 30 % less, respectively, than those of capitula formed during primary flowering. These reductions appear to result from restricted availability of resources. Large and small achenes have similar dispersal characteristics and possess similar germination potential. However, large achenes produce seedlings that are capable of emerging from greater burial depths, providing the resulting plants with a potential advantage. The normal flowering period coincides with the optimum time of year for flowering and fruiting in the south of Spain, and only if rainfall lasts longer than usual does secondary flowering occur. Secondary flowering extends the normal flowering and fruiting periods, thereby providing a supplementary crop of smaller, yet viable, fruits. It can be considered to be an adaptive response to the unpredictable Mediterranean climate, optimizing the use of available resources.
Key words: Centaurea eriophora, Asteraceae, secondary flowering, achene mass variation, resource allocation, germination, growth.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Seeds are assumed to be highly stable in mass relative to other, more plastic, plant organs. Plants tend to produce seeds of a size that optimizes the investment; as a result, they usually vary little in size (Harper et al., 1970). Seeds smaller than the optimal size may be of low fitness or inviable, whereas investment in large seeds may waste resources that could be used to produce more seeds.
The constancy of seed size has been ascribed to trade-offs between seed number and mass (Stanton, 1984a; Lalonde and Roitberg, 1989; Venable, 1992). Thus, in the presence of limited resources, plants tend to reduce the number of seeds they produce rather than their mass. Contrary to these assertions, the mass changes observed in many species suggest that they have a limited ability to vary seed size. In fact, many species exhibit substantial changes in seed mass among different populations, within a population, or even on the same plant. Factors inducing changes in seed mass include genetic differences (Stanton, 1984b; Temme, 1986), pollen availability (Bertness and Shumway, 1992) or pollen origin (Lalonde and Roitberg, 1989; Vaughton and Ramsey, 1997). Other factors are related to changes in resource availability, including defoliation (Stephenson, 1980; Crawley and Nachapong, 1985; Vaughton and Ramsey, 1997, 1998), environmental changes (Pitelka et al., 1983), the position of seeds within the fruit or on the plant (McGinley, 1989; Rocha and Stephenson, 1990; Winn, 1991; Obeso, 1993; Maxwell et al., 1994; Navarro, 1996; Vaughton and Ramsey, 1997; Méndez, 1997), the number of seeds produced by each fruit (Wulff, 1986; Winn, 1991), seasonal decline (Cavers and Steel, 1984; Winn, 1991; Obeso, 1993; Meyer, 1997; Vaughton and Ramsey, 1998) and plant density (Matthies, 1990; Ruiz de Clavijo and Jiménez, 1998). Within-plant and between-plant patterns of variation suggest that smaller seeds are produced when resources are limited.
Since intraspecific variability in seed mass is regarded as an important aspect in the evolution of angiosperms, it has received special attention on account of the potential adaptive consequences of producing seeds of different mass. In fact, variation in seed mass can have a variety of implications for germination (Wulff, 1973, 1986; Pitelka et al., 1983; Hendrix, 1984; Ruiz de Clavijo, 1995; Andersson, 1996), dispersal (Morse and Schmitt, 1985; Matlack, 1987), the ability to emerge from different burial depths (Maun and Lapierre, 1986; Yanful and Maun, 1996; Ruiz de Clavijo, 2001), seedling vigour (Pitelka et al., 1983; Stanton, 1984a; Wulff, 1986; Ruiz de Clavijo, 1995, 2001; Méndez, 1997; Eriksson, 1999) and the competitive ability of the resulting plants (Weis, 1982; Gross, 1984; Jurado and Westoby, 1992; Salonen and Suhonen, 1995; Ruiz de Clavijo and Jiménez, 1998; Vaughton and Ramsey, 1998). All of these factors can influence population establishment.
The considerable within-individual variability in capitulum size, and achene size and mass, observed in wild and cultivated plants of Centaurea eriophora led us to study the causes and consequences of such variation. The specific objectives of the study were to: (1) determine natural within-individual variation in capitulum size and its relationship to flowering time; (2) examine variation in fruit number, size and mass as a function of capitulum size; (3) identify the causes of the variation; and (4) determine the influence of achene mass on dispersal, germination, emergence and vigour of the resulting seedlings.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Centaurea eriophora L. (Asteraceae) is an annual weed that occurs in the south of the Iberian Peninsula, north-west Africa and the Canary Islands, and has recently been introduced to Israel (Witztum, 1989). It grows on calcareous soils on roadsides and in open arid spaces. Following a rosette stage, plants develop an erect stem bearing leaves with lateral branches of different orders, ending in capitula also of different orders (primary, secondary, tertiary and small capitula). An individual plant can produce capitula of two sizes yielding achenes that also differ in size (large and small achenes). Capitulum bracts are spiny and coated with a dense white arachnoidal indumentum. Flowers are yellow, the peripheral ones being sterile, but all others are fertile and hermaphroditic. The achenes produced by each capitulum are similar, possess a pappus of bristles that causes them to move upwind (Witztum et al., 1996) and a well-developed elaisome (oil-containing appendage).
The experimental part of the study was conducted on plants cultivated at ambient temperature in a glasshouse at Córdoba, in south-western Spain. Observations of growth, phenology and capitulum production were also made in a natural population located near the village of Jauja, in the province of Córdoba, during 1998–99. Córdoba has a typical Mediterranean climate with wet, mild winters and long, dry, hot summers.
Plant growth and capitulum and achene production
In June 1998, 50 ripe C. eriophora capitula were collected at random from the natural population and their achenes extracted. In November 1998, 40 randomly chosen achenes were sown in pots 15 cm deep and 16 cm in diameter, and cultivated in a glasshouse. Vegetative growth and the production, chronology and phenology of capitula of different orders were monitored. Once ripe, but before achene dispersal, capitula were collected and their position on the plant (order), diameter and weight were recorded. A sample consisting of 30 randomly chosen capitula of each order was used to count the number of fertile flowers and achenes per capitulum to calculate percentage fruit set. A second sample of 50 randomly chosen achenes of each capitular type was used to determine achene weight, achene dimensions and pappus length. Forty achenes were sown individually in similarly sized pots in February 1999 to determine whether the sizes of capitula and achenes were influenced by the time that they were produced. All pots were watered regularly until mid-July and supplied with liquid inorganic fertilizer on a monthly basis.
Achene dispersal
The potential of the achenes to be dispersed by wind was assessed by measuring their rates of fall in still air. Using a digital chronometer, the time taken for an achene to fall 2 m in a tightly closed room was measured. Mean fall rates were obtained by measuring 40 achenes of each type, recording the fall time for each achene three times.
Germination
To check for differences in germination between large and small achenes, achenes were germinated under either controlled light and temperature conditions or under ambient conditions in a glasshouse. The former test was performed in a growth chamber using achenes from cultivated plants. Twenty healthy, ripe achenes were placed in Petri dishes containing two layers of filter paper soaked in distilled water. Five different constant-temperature regimes (5, 10, 15, 20 and 25 °C) were used (12 h photoperiod), with six dishes (replicates) per achene type and temperature. Dishes were inspected over 1 month and the number of germinated achenes recorded. Achene viability was determined at the end of germination tests. Intact, non-germinated achenes posessing a normal embryo were counted as viable, in contrast to disorganized and necrotic, non-viable achenes. Germination percentages were calculated from the total number of viable achenes.
Germination tests were also performed in a glasshouse under ambient lighting and temperature conditions during 1998–2000. Early in November 1998, 20 previously selected achenes of each type were distributed over each of ten soil trays (replicates). The trays were watered regularly until late May 1999 and the number of germinated achenes recorded. Achenes that had not germinated were left in the trays, which were again watered regularly from November 1999 until May 2000. The number of achenes that germinated during the second year was recorded.
Emergence
The ability of seedlings from large and small achenes to emerge from different burial depths was determined by burying ten newly germinated achenes of each type at 1, 2, 3, 4, 5 and 6 cm in soil trays. Ten trays (replicates) per achene type and burial depth were used. Trays were examined over 1 month and the number of emerged seedlings recorded.
Seedling growth
To compare growth of seedlings from large and small achenes, 20 newly germinated achenes of each type were sown in pots. After 10 d, the length and width of cotyledons was measured to calculate their area. After 1 month, the above-ground vegetative portion of the plants was harvested and the number, length and width of all leaves recorded. Total dry weight of leaves was measured following drying in an oven at 60 °C for 48 h. Twenty plants from each type of achene were also cultivated in pots to compare the onset of flowering and capitulum production.
Data analysis
Statistical analysis was performed using Statistica (StatSoft, 1996). Data on capitulum, achene and seedling characteristics, and on the fall rate of achenes were compared by one-way ANOVA and differences among means tested using Tukey’s test. Achene germination data under different temperatures in the growth chamber were analysed by two-way ANOVA.
The variance of data on germination in the glasshouse, and emergence, was heterogeneous and the data were not normally distributed. As arcsine-square root transformation did not reduce the deviation from normality, the data were analysed using the Mann–Whitney U-test. Untransformed means (± s.d.) are presented in the text and tables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant growth and capitulum and achene production
Following germination of the achenes sown in the glasshouse in November, a basal leaf rosette was formed from which the main stem developed by late March. Capitula formed in an asynchronous manner. Each plant produced successive capitula of different orders on lateral branches of successive order. The main stem developed a terminal primary capitulum (Fig. 1) that flowered in late April. At the same time that the achenes produced by these capitula ripened, two or three primary lateral branches developed (both immediately below and on the axils of the superior leaves) with a pseudo-dichotomous appearance. Terminal capitula were produced and they flowered around mid-May. Below each secondary capitulum, two secondary lateral branches usually developed. Terminal tertiary capitula were produced and they flowered in late May or early June (Fig. 2). As primary capitula ripened, leaves of the basal rosette senesced. After tertiary capitula ripened, cauline leaves senesced and remained marcescent on the stems. Primary, secondary and tertiary capitula constituted the primary flowering.
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A second, later, flowering sometimes occurred during June and in early July, once tertiary capitula were ripe (Fig. 2). The, by then, almost senescent plants produced a variable number of small capitula located on the ends of short (1–2 cm) lateral branches that developed on first- or second-order branches (Fig. 1) and that bore several small leaves each. Following this flowering, the small leaves persisted until the achenes ripened and the plants eventually senesced by mid-July. The small capitula were always the last to be produced and constituted the secondary flowering. The time lag between production of the different types of capitula prevented the simultaneous flowering of capitula of different orders on the same plant, even though there was a slight overlap of the flowering time of the different types of capitulum (Fig. 2).
Primary, secondary and tertiary capitula were very similar. All were sub-spherical and of similar diameter (Table 1). Although differences were slight, primary capitula produced fewer fertile flowers than did secondary and tertiary capitula, but had a greater percentage fruit set. Flower anthesis in each capitulum was highly synchronous. The mean duration (± s.d.) of anthesis in primary, secondary and tertiary capitula was 2·9 ± 0·53, 2·9 ± 0·83 and 2·7 ± 0·60 d, respectively. Secondary capitula weighed slightly more and they produced more achenes on average than did primary and tertiary capitula (Table 1).
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Small capitula differed markedly to large capitula. Most formed during the second half of June (roughly 1 month later than tertiary capitula). The small capitula were sub-ovoid, twice as long as they were wide. They were normally produced in greater numbers and had a diameter about half that of the other capitula types (Table 1). In addition, they produced about 66 % fewer flowers and 70 % fewer achenes. The duration of anthesis (1·3 ± 0·45 d) was about half that of the other capitula, and their percentage fruit set was less (Table 1).
There were no significant weight differences among the achenes produced by primary, secondary and tertiary capitula (large achenes) (Table 2). Because flowers in each capitulum reached anthesis synchronously, fruits also ripened simultaneously on each. Achene ripening lasted 30·4 ± 1·91 d (range 27–33 d, n = 20), 25·0 ± 2·24 d (range 22–28 d, n = 20) and 25·6 ± 2·37 d (range 22–30 d, n = 20) in primary, secondary and tertiary capitula, respectively. Achenes produced by small capitula (small achenes) weighed about 30 % less (Table 2) and they ripened more quickly (22·0 ± 4·32 d, range 18–30 d, n = 20).
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The pattern of variation for capitulum production was uniform in all plants cultivated in the glasshouse and was independent of sowing time. In pots sown in late February, primary capitula flowered in mid-May, secondary capitula in late May, tertiary capitula in mid-June and the small capitula started flowering in early July. Flowering of small capitula on the plants sown in November coincided with flowering of tertiary capitula on the plants sown in February.
Flowering of large and small capitula was not always observed in plants in the wild. In 1998, most of the plants in the natural population produced both types of capitulum, but in 1999 they produced large capitula only.
Dispersal
The fall rate of large achenes was significantly greater (P < 0·01; Tukey’s test) than that of small achenes (2·18 ± 0·078 vs. 2·07 ± 0·094 m s–1). Since height differences between different capitulum types were minimal (Fig. 1), this factor would not have been important in dispersal.
Germination
Germination tests conducted in a growth chamber at different temperatures revealed similar percentage germination at each temperature in the two achene types (Table 3). Two-way ANOVA (temperature and achene type as fixed factors) of final germination indicated no differences in germination between large and small achenes, but a significant effect of temperature on germination. There was a non-significant interaction between temperature and achene type (Table 4).
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In glasshouse tests, 41·7 % (range 20–67 %, s.d. = 16·65) of the small achenes and 36·4 % (range 20–55 %, s.d. = 10·56) of the large achenes germinated in the first year; differences were not significant (P < 0·05, Mann–Whitney U-test). Cumulative germination curves (Fig. 3) revealed that the onset of germination and germination rate were similar in both types of achene. The proportions germinating by the second year were 83·5 % (range 70–95 %, s.d. = 7·09) and 79·0 % (range 71–89 %, s.d. = 5·97) for the large and small achenes, respectively, and did not differ significantly (P < 0·05, Mann–Whitney U-test). Percentage viability was similar in the two achene types (98·8 ± 5·61 and 97·5 ± 8·84 % for large and small achenes, respectively).
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Emergence
Seedlings from large achenes emerged from greater burial depths than those from small achenes (Table 5). All seedlings emerged successfully from achenes buried 1 or 2 cm deep, but for burial depths greater than 2 cm, the percentage emergence was significantly greater for large achenes. No seedlings emerged from below 5 cm.
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Seedling growth
The area of cotyledons of 10-d-old seedlings from large achenes was significantly greater than that of seedlings from small achenes (Table 6). Differences between the types of seedling decreased during growth, and 1-month-old seedlings exhibited no difference in the number and area of leaves or plant dry weight (Table 6). There was no difference in the onset of flowering or in the production of capitula by adult plants of either type.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Centaurea eriophora plants can have two successive flowering periods if wet conditions last longer than usual. During the first (primary) flowering that occurs between late April and early June, primary, secondary and tertiary capitula of similar size are produced, which yield achenes of similar mass. After this period, leaves gradually senesce, regardless of whether environmental conditions remain favourable, and achenes are dispersed from mid-June.
Secondary flowering can occur during June and the first half of July if environmental conditions are favourable. In this secondary flowering a variable number of small capitula are produced. They are more than 50 % smaller in diameter and produce 70 % fewer achenes that are 30 % lighter than those from the first flowering. These small capitula grow on plants that have almost senesced, at the end of lateral branches bearing a few, very small leaves. The small branches that bear these capitula function as autonomous units, providing the resources required for the capitula to develop. However, since the branches have a limited ability to supply the capitula, they are small and produce fewer, lighter achenes than those of the first flowering. The lower mass of achenes from the small capitula suggests that there is a failure to maintain achene weight by controlling numbers.
In some species, within-individual mass differences among seeds are induced by environmental factors, such as restrictions in resource availability as the growing season develops (Hendrix, 1984; Winn, 1991; Obeso, 1993; Vaughton and Ramsey, 1998) or by changes in other factors (e.g. lighting) that affect plant growth (Pitelka et al., 1983). The present results suggest that these cannot be the factors inducing mass differences among C. eriophora achenes. Plants were cultivated under constant conditions in a glasshouse and were supplied with water and fertilizer on a regular basis until the end of July; thus, resources were not limiting. Furthermore, the occurrence of secondary flowering does not depend on environmental light and temperature conditions since plants in primary (sown in February) and in secondary (sown in November) flowering coexisted in the glasshouse.
The results indicate that the production of capitula of different size and achenes of different mass arise from intrinsic features of the plants, such as their inability to supply sufficient resources to the capitula owing to the small number of leaves. However, the resources reaching the capitula are sufficient for the production of an additional crop of viable, though smaller, fruits.
Several species have been found to produce an excessive number of flowers, some of which inevitably fail to set fruit owing to the limited availability of resources. Flower abortion is a strategy used by plants in the adjustment to available resources. In variable and unpredictable environments, this strategy can be advantageous despite the loss of resources to aborted flowers (Bazzaz, 1997). In C. eriophora plants, primary flowering occurs during the most favourable period for plant growth in this Mediterranean area (April, May and early June). In this period plants ramify in an ordered manner and develop branches of up to second order, and capitula of up to third order that are similar in size, and yield achenes in similar numbers and of similar weight. The number of capitula produced by plants cultivated under controlled conditions in a glasshouse during primary flowering was very constant (Table 1) yet, in wild plants, the number of capitula was variable and was related to plant growth.
In the south of the Iberian Peninsula, spring rains usually end in May and are followed by a dry period that spans the entire summer, ending with the autumn rains (in October and November). In a typical year, wild plants of C. eriophora exhibit primary flowering only, and once achenes ripen around mid-June, the plants die. However, an extended rainy period provides adequate soil moisture, and secondary flowering occurs in seemingly senescent plants. The number of capitula thus formed depends on the duration of this period of water availability. Plants cultivated in the glasshouse were watered until mid-July and all exhibited secondary flowering, in contrast to the natural populations where it was found to depend on rainfall in that particular year. The spring of 1998 was very wet in the south of the Iberian Peninsula, with frequent rains during April, May and the first week of June. By the end of May, the surplus of rain with respect to a normal year was greater than 400 l m–2. Virtually all plants in the wild population exhibited secondary flowering and produced small capitula. In contrast, 1999 was an extremely dry year with virtually no rain falling during April and May; the annual precipitation deficit by the end of May exceeded 300 l m–2. The plants, which were underdeveloped, produced only some of the typical capitula of primary flowering and none of secondary flowering.
The production of seeds of different mass is commonly related to differences in other properties of the seeds, such as germination potential, competitive ability, dispersal or ability to emerge following burial. Centaurea eriophora exhibits no differences in germination between large and small achenes. Only approx. 40 % of achenes germinated under ambient conditions during the first year and 80 % had germinated by the end of the second. This suggests the presence of a soil bank of long-lived achenes, which is typical of many species that grow in variable, unpredictable habitats (Thompson and Grime, 1979).
Dispersal characteristics were also similar in large and small achenes. Because they fall rapidly (approx. 2 m s–1) from low heights (the tallest plants are less than 1 m), achenes, as in other Centaurea species (Andersen, 1993), are unlikely to be dispersed over long distances by the wind. The structure of the pappus facilitates upwind motion (Witztum et al., 1996). However, it is possible that the most effective dispersal mechanism for both types of achene is by ants attracted to their elaisome. Alternatively, achenes may be dispersed via a passive ballistic mechanism (Van der Pijl, 1972; Andersen, 1993).
Seedlings from large achenes are initially more vigorous because they possess larger cotyledons than those from small achenes. The differences, however, disappear rapidly, and adult plants of both types cultivated in a glasshouse performed similarly. The initial differences in growth between seedlings may result in different performances in the field, where various environmental stress conditions could have differential effects on the two types of seedling. On the other hand, the fact that seedlings from large achenes can emerge from greater burial depths could favour them over those from small achenes.
The succession of two flowering periods in C. eriophora may constitute an adaptation to the unpredictable Mediterranean climate, leading to more efficient use of available resources, provided that favourable conditions persist (i.e. soil moisture is adequate). The strategy adopted by these plants involves prolonging the flowering and fruiting periods, thereby generating an additional crop of viable, although smaller, achenes. In annual plants an increase in seed set is advantageous. Here, the additional crop raised the overall number of achenes by 42 % and the total achene biomass by 29 % in cultivated plants. The only disadvantages of the small achenes relative to those produced during primary flowering are a reduced ability to emerge from burial depths greater than 3 cm and the fact that they produce plants that are initially less vigorous and that might perform poorly under environmental stress.
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ACKNOWLEDGEMENTS |
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The author is grateful to Dr S. Talavera (University of Seville) for comments on the manuscript and to Dr P. Cariñanos (University of Córdoba) for help in the preparation of the manuscript. This study was partially funded by Spain’s DGICYT within the framework of Project PB95-0019.
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LITERATURE CITED |
|---|
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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-
Andersen MC. 1993. Diaspore morphology and seed dispersal in several wind-dispersed Asteraceae. American Journal of Botany 80: 487–492.[CrossRef]
Andersson S. 1996. Seed size as a determinant of germination rate in Crepis tectorum (Asteraceae): evidence from a seed burial experiment. Canadian Journal of Botany 74: 568–572.
Bazzaz FA. 1997. Allocation of resources in plants: state of the science and critical questions. In: Bazzaz FA, Grace J, eds. Plant resource allocation. San Diego, London: Academic Press, 1–37.
Bertness MD, Shumway SW. 1992. Consumer driven pollen limitation of seed production in marsh grasses. American Journal of Botany 79: 288–293.[CrossRef]
Cavers PB, Steel MG. 1984. Patterns of change in seed weight over time on individual plants. American Naturalist 124: 324–335.[CrossRef]
Crawley MJ, Nachapong M. 1985. The establishment of seedlings from primary and regrowth seeds of ragwort (Senecio jacobeae). Journal of Ecology 73: 255–261.[CrossRef]
Eriksson O. 1999. Seed size variation and its effect on germination and seedling performance in the clonal herb Convallaria majalis. Acta Oecologica 20: 61–66.[CrossRef]
Gross KL. 1984. Effects of seed size and growth form on seedling establishment of six monocarpic perennials. Journal of Ecology 72: 369–387.[CrossRef]
Harper JL, Lovell PH, Moore KG. 1970. The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1: 327–356.
Hendrix SD. 1984. Variation in seed weight and its effects on germination in Patinaca sativa L. (Umbelliferae). American Journal of Botany 71: 795–802.[CrossRef]
Jurado E, Westoby M. 1992. Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology 80: 407–416.[CrossRef]
Lalonde RG, Roitberg BD. 1989. Resource limitation and offspring size and number trade-offs in Cirsium arvense (Asteraceae). American Journal of Botany 76: 1107–1113.[CrossRef]
McGinley MA. 1989. Within and among plant variation in seed mass and pappus size in Tragopogon dubius. Canadian Journal of Botany 67: 1298–1304.
Matlack GR. 1987. Diaspore size, shape, and fall behaviour in wind-dispersed plant species. American Journal of Botany 74: 1150–1160.[CrossRef]
Matthies D. 1990. Plasticity of reproductive components at different stages of development in the annual plant Thlaspi arvense L. Oecologia 83: 106–116.
Maun MA, Lapierre J. 1986. Effects of burial by sand on seed germination and seedling emergence of four dune species. American Journal of Botany 73: 450–455.[CrossRef]
Maxwell CD, Zobel A, Woodfine D. 1994. Somatic polymorphism in the achenes of Tragopogon dubius. Canadian Journal of Botany 72: 1282–1288.
Méndez M. 1997. Sources of variation in seed mass in Arum italicum. International Journal of Plant Sciences 158: 298–305.[CrossRef]
Meyer SE. 1997. Ecological correlates of achene mass variation in Chrysothamnus nauseosus (Asteraceae). American Journal of Botany 84: 471–477.[Abstract]
Morse DH, Schmitt J. 1985. Propagule size, dispersal ability, and seedling performance in Asclepias syriaca. Oecologia 67: 372–379.[CrossRef]
Navarro L. 1996. Fruit-set and seed weight variation in Anthyllis vulneraria subsp. vulgaris (Fabaceae). Plant Systematics and Evolution 201: 139–148.[CrossRef]
Obeso JR. 1993. Seed mass variation in the perennial herb Asphodelus albus: sources of variation and position effect. Oecologia 93: 571–575.[CrossRef]
Pitelka LF, Thayer ME, Hansen SB. 1983. Variation in achene weight in Aster acuminatus. Canadian Journal of Botany 61: 1415–1420.
Rocha OJ, Stephenson AG. 1990. Effect of ovule position on seed production, seed weight and progeny performance in Phaseolus coccineus L. (Leguminosae). American Journal of Botany 77: 1320–1329.[CrossRef]
Ruiz de Clavijo E. 1995. The ecological significance of fruit heteromorphism in the amphicarpic species Catananche lutea (Asteraceae). International Journal of Plant Sciences 156: 834–833.[CrossRef]
Ruiz de Clavijo E. 2001. The role of dimorphic achenes in the biology of the annual weed Leontodon longirrostris. Weed Research 41: 275–286.[CrossRef]
Ruiz de Clavijo E, Jiménez MJ. 1998. The influence of achene type and plant density on growth and biomass allocation in the heterocarpic annual Catananche lutea (Asteraceae). International Journal of Plant Sciences 159: 637–647.[CrossRef]
Salonen V, Suhonen J. 1995. Effects of seed weight on growth, reproduction and competitive ability of Linum usitatissimum seedling. Annales Botanici Fennici 32: 101–106.
Stanton ML. 1984a. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65: 1105–1112.[CrossRef]
Stanton ML. 1984b. Developmental and genetic sources of seed weight variation in Raphanus raphanistrum L. (Brassicaceae). American Journal of Botany 71: 1090–1098.[CrossRef]
StatSoft Inc. 1996. Statistica for Windows. 5·1 (Computer program manual). Tulsa, USA, StatSoft Inc.
Stephenson AG. 1980. Fruit set, herbivory, fruit reduction, and the fruiting strategy of Catalpa speciosa (Bignoniaceae). Ecology 61: 57–64.[CrossRef]
Temme DH. 1986. Seed size variability: a consequence of variable genetic quality among offspring? Evolution 40: 414–417.[CrossRef]
Thompson K, Grime JP. 1979. Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology 67: 893–921.[CrossRef]
Van der Pijl L. 1972. Principles of dispersal in higher plants. Berlin: Springer-Verlag.
Vaughton G, Ramsey M. 1997. Seed mass variation in the shrub Banksia spinulosa (Proteaceae): resource constraints and pollen source effects. International Journal of Plant Sciences 158: 424–431.[CrossRef]
Vaughton G, Ramsey M. 1998. Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). Journal of Ecology 86: 563–573.[CrossRef]
Venable DL. 1992. Size-number trade-offs and the variation in seed size with plant resource status. American Naturalist 140: 287–304.[CrossRef][ISI]
Weis IM. 1982. The effects of propagule size on germination and seedling growth in Mirabilis hirsuta. Canadian Journal of Botany 60: 1868–1874.
Winn AA. 1991. Proximate and ultimate sources of within-individual variation in seed mass in Prunella vulgaris (Lamiaceae). American Journal of Botany 78: 838–844.[CrossRef]
Witztum A. 1989. Contributions to the flora of Israel and Sinai. IV. Centaurea eriophora L. in Israel. Israel Journal of Botany 38: 59–62.
Witztum A, Schulgasser K, Vogel S. 1996. Upwind movement of achenes of Centaurea eriophora L. on the ground. Annals of Botany 78: 431–436.
Wulff R. 1973. Intrapopulational variation in the germination of seeds in Hyptis suaveolens. Ecology 54: 646–649.[CrossRef]
Wulff R. 1986. Seed size variation in Desmodium paniculatum. II. Effects on seedling growth and physiological performance. Journal of Ecology 74: 99–114.[CrossRef]
Yanful M, Maun MA. 1996. Effects of burial of seeds and seedlings from different seed sizes on the emergence and growth of Strophostyles helvola. Canadian Journal of Botany 74: 1322–1330.
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