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Reproductive Biology |
Área de Botánica, Departamento de Biología Molecular e Ingeniería Bioquímica, Universidad Pablo de Olavide 41013 Sevilla, Spain
Received for publication 7 September 2007. Accepted for publication 13 February 2008.
ABSTRACT
Inflorescence architecture directly determines variations in floral traits and fecundity. Disentangling these patterns of variation is crucial to understanding intraplant variation, which sometimes is directly attributed to competition for resources with developing fruits. The dichasial cymes of Silene acutifolia were experimentally manipulated in the field to analyze whether the declines in petal size, ovule number, fruit set, and seed/ovule ratio along the inflorescence are constrained by ontogenetic development or are phenotypically plastic in response to environmental changes. At the same time, the level of pollen deficit was measured on different positions of the dichasia. The results showed clearly that all measured variables were more influenced by architecture than by resource competition with developing fruits; the removal of central (basal) and primary lateral flowers in the dichasia did not increase either the measures of floral characters or fecundity. On the other hand, although most of the decline in fecundity was due to architectural effects, there was also a pollen limitation, dependent to some degree on inflorescence position, which was probably due to lower pollen availability in the population when secondary flowers are in the female phase.
Key Words: architectural effects • Caryophyllaceae • fruit set • Iberian Peninsula • limb length • ovule number • resource competition • seed/ovule ratio
Intraplant variation in phenotypic floral traits and fecundity is a very common phenomenon in plants, although studies have predominantly focused on the interplant level. Because of the modular structure of plants, every individual may have many different floral axes, which often act as semiautonomous structural and functional subunits (Watson and Casper, 1984
; de Kroon et al., 2005). In general, the number of modules is important in determining the number of meristems available to become new vegetative or reproductive modules (Preston, 1998). An important part of this intraindividual variation is often located at the level of the inflorescence (Diggle, 1995, Diggle, 2003), which sometimes absorbs most of the variation (Winn, 1991). In a study introducing seed variation among individuals, among inflorescences, and within inflorescences, Winn found most of the variation located within inflorescences. This intrainflorescence variation has been reported especially in relation to fruit maturation and seed production, with a high probability of maturation of early-formed fruits or those located closer to the sources of nutrients and photosynthates (Stephenson, 1981; Lee, 1988; Herrera, 1991; Obeso, 1993; Guitián and Navarro, 1996; Medrano et al., 2000; Wolfe and Denton, 2001; reviewed in Diggle, 2003; Pritchard and Edwards, 2005). These studies usually examine only variations in the number of fruit and/or seeds with respect to the number of flowers produced, considering flowers as morphologically identical (Herrera, 1991), or focus in gender differences along the inflorescence axis (Ashman and Hitchens, 2000; Ashman et al., 2001). However, many plants also vary in floral size within an inflorescence or in the number of ovules or pollen independently of the sexual condition of the flowers (Wolfe, 1992; Vallius, 2000; reviewed in Diggle, 2003; Bateman and Rudall, 2006). Such is the case for the hermaphrodite Silene acutifolia.
This phenotypic variation may have originated from environmental factors, which can be extrinsic and/or intrinsic. Extrinsic factors include pollinators, herbivores, predators, and diseases, which are more likely to influence the flowers randomly. The intrinsic include competition for resources, especially photosynthates and hormones (Lloyd, 1980; Stephenson, 1981; Lee, 1988), and are more likely to affect inflorescences systematically. The effect of environmental factors that influence flowers nonrandomly would be difficult to distinguish in its effect from architecture (Wolfe, 1992; Diggle, 1994, Diggle, 1995, Diggle, 1997, Diggle, 2002; Watson et al., 1995). Therefore, architectural effects can mask plasticity, making necessary the analysis of architectural variation to understand the sources of variation in floral form and function (Diggle, 2003). One hypothesis to explain architectural variation effects is the decline in vascular tissue along the length of an inflorescence (Wolfe and Denton, 2001). However, this cannot be the only reason, and we have to search for a more general explanation (Diggle, 2003).
One important reason to analyze variation is that architecture and environmental variation can complicate the measure of their genetic components. In addition, selection may act on variability as a trait. In S. marina, Mazer and Delesalle (1996a, b) found genetic variation among populations in the degree to which phenotype changes over time and proposed that the degree of temporal variation in floral trait expression may itself be a trait under genetic control and open to natural selection. On the other hand, selection may favor specialization of flowers according to their position. As an example, on sequentially blooming plants with protandrous flowers, later flowers may specialize in male function. In this type of plant, the opportunity for male flowers to sire seeds may vary among flowers, which may imply that later flowers in the inflorescence do not find enough pollen when they are in female phase and specialize in male function (Bawa and Webb, 1984; Brunet and Charlesworth, 1995; Brunet, 1996).
Silene has high intraspecific variation in floral form and function. Different species of this genus are currently the organisms of choice for a variety of evolutionary issues, including the origin of sex chromosomes (Filatov and Charlesworth, 2002; Lengerova et al., 2003; Filatov, 2005) and the evolution of floral dimorphism, gynodioecy, and dioecy (Taylor et al., 2001; Delph et al., 2002). Therefore, comprehension of the causes of floral variation is fundamental. As an example, variation in floral traits resulting from sexual dimorphism could be confounded with variation resulting from architectural effects and/or competition for resources. On the other hand, intraspecific variation in Silene is not restricted to those species with sexual dimorphism and is also present in hermaphrodites. As shown in a previous study (Buide, 2004), the hermaphrodite S. acutifolia has substantial intrainflorescence variation in the number of ovules per flower, fruit set, number of seeds per fruit, seed mass, and seed germination, which was consistent in all populations and years. In this work, the causes of flower and fruit variation were analyzed for S. acutifolia in an experiment carried out in natural populations, which permitted the analysis of intrinsic as well as extrinsic (pollen limitations) factors by means of experimental manipulations. The first aim of this paper was to measure the magnitude of intraplant variation in ovule number per flower, limb length (as a measure of corolla length), fruit set, and seed/ovule ratio in natural conditions. The second aim was to determine which part of the fruit set and seed/ovule ratio differences were due to pollen limitations. Finally, the third aim was to explain the remaining intrainflorescence variation when pollen limitations are excluded. The tested hypothesis was that this variation was due to either inflorescence architecture and/or resource limitation resulting from competition with developing fruits. To do this, I compared the variation in the different traits measured in plants whose central and primary lateral flowers of the dichasia were removed with plants whose central and primary lateral flowers received supplementary pollination.
MATERIALS AND METHODS
Plant and study area
Silene acutifolia Link ex Rohrb., a polycarpic herb with a rosette of basal leaves, grows typically in rocky habitats. It is endemic to northwest Spain and north and central Portugal (Talavera, 1990). The purplish-pink flowers are hermaphroditic and protandrous, although the temporal separation between the male and female phases is not complete, making self-pollination possible; geitonogamous crosses are common, but they do not reduce either fruit or seed set (Buide and Guitián, 2002). In addition, there were low levels of inbreeding depression (0.019), calculated based on the relationship between the seed/ovule ratio of self-pollinated flowers (including geitonogamy) and of cross-pollinated flowers (Buide and Guitián, 2002). The flowering peak is in April or May, depending on the year and population (Buide et al., 2002).
Flowers are borne in dichasial cymes (Fig. 1). Typical inflorescences have a central (basal) flower with one flower on each side (primary laterals), which also have two lateral flowers (secondary laterals). The flowers have five free petals forming a functional tube enclosed by the tubular calyx. The calyx length is a measure of the access distance to the nectar, which in Caryophyllaceae is located in a disc at the base of the stamens. The petals have a claw, enclosed by the calyx, and a limb. The claw has a small fringe at the top. Because claws are inside the calyx tube, the attractive part of the corolla is the limb (Fig. 1). The number of flower stems varies greatly among plants, and as a result, the number of open flowers also varies. The main pollinators are long-tongued insects, including Hymenoptera, Lepidoptera, and Diptera, although the composition and visitation frequencies of pollinators vary among years. Pollinators are needed if the fruit and seed/ovule ratios are to reach the highest levels, and pollen limitations have been detected in this plant in some but not all years of study (Buide, 2006).
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Experimental manipulations (Fig. 2)
Treatment A (flower removal and pollen supplementation): central (basal) and primary (lateral) flowers were removed and measured when they opened (male phase). Secondary lateral flowers developed later and were not open when the central and primary flowers were removed. Secondary (lateral) flowers were also measured in the male phase to avoid differences in size because of floral age. Secondary flowers were supplementary hand-pollinated with outcrossed pollen at the female stage, and fruit and nonfruiting flowers were collected.
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Treatment C (flower removal): central (basal) and primary (lateral) flowers were measured and removed as in treatment A. Secondary (lateral) position flowers were also measured, but left to natural pollination. All remaining fruits and nonfruiting flowers were collected.
For the controls (D), all flowers were measured in the male phase and not manipulated.
Petal limb length was used as a representative measure of corolla size to avoid floral damage during manipulations (Fig. 1). Measures were made to the nearest 0.01 mm using Mitutoyo (Andover, UK) calipers. Flowers and fruits were frozen, and the number of ovules, seeds, and aborted ovules were counted with the aid of a dissecting microscope. Fruit set was calculated as the percentage of fruits in relation to total flowers produced (matured fruits and nonfruiting flowers). The total number of flowers produced by the plant can be calculated because nonfruiting flowers remain on the plant. Fruits were dissected, and the number of seeds and aborted ovules were counted. The seed/ovule ratio was calculated as the percentage of seeds in relation to the total number of ovules.
Data treatment
Pollen limitations were tested by comparing fruit set and seed/ovule ratio between treatment B and control inflorescences.
Following Diggle (1997), the comparisons in Table 1 were made to detect architectural and/or resource limitations resulting from developing fruits (see also Fig. 2). Total variation was measured within treatment B plants because fruit and seed production was assured with supplementary pollination. Thus, maximal differences should be found between central and secondary flowers/fruits of these plants. Architectural effects were measured by comparing central and secondary flowers in the "no competing fruit" treatments (A and C). Because central and primary flowers of treatments A and C were removed and consequently did not produce fruits, architectural effects in fruit and seed/ovule ratio were evaluated by comparing CB (central position, treatment B) and SA (secondary position, treatment A) fruits. Finally, the effects of resource competition resulting from developing fruits were measured by comparing the secondary flowers of "no competing fruit" treatments with the same order flowers in treatment B. As before, the central fruits of treatment B were used for the fruit set and seed/ovule ratio (Fig. 2).
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To analyze the effect of pollen supplementation and inflorescence position in fruit and the seed/ovule ratio, I performed analyses of variance by fitting generalized linear models to the data, with quasibinomial errors to avoid overdispersion, and logit link (fruit set) or probit link (seed/ovule ratio) (McCullagh and Nelder, 1989). Calculations were made using the program R 2.4.1 (R Development Core Team, 2006).
Comparisons between central (basal) and secondary (lateral) positions to measure total variation, architectural effects, and resource competition were made with t tests in SPSS 14.0.1.
RESULTS
Intrainflorescence variation in floral traits
The median of petal limb length of control flowers was 10.2 mm for flowers at the central (basal) position (50% of limb lengths: 9.8–11.1 mm), 9.3 mm for primary (lateral) flowers (8.8–9.8 mm), and 8.8 mm for secondary (lateral) flowers (8.3–9.3 mm) (Fig. 3). The median of ovules per flower was 57 for flowers at the central (basal) position (50% of ovules: 53.5–60), 51 for primary (lateral) flowers (47.8–56), and 45 for secondary (lateral) flowers (41–49) (Fig. 3).
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Testing the causes of intrainflorescence variation
Pollen limitation
There was a significant increment in fruit set with pollen supplementation (treatment B), a significant reduction with position, and no significant interactions were found (Table 2). However, central (basal) flowers did not increase fruit set with pollen supplementation (Fig. 4A), and the highest differences in fruit set between control and supplementary-pollinated flowers corresponded to secondary (lateral) flowers (17%).
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Resource limitations vs. architectural effects
The total intrainflorescence variation was calculated by subtracting the mean value of central flowers or fruits in treatment B from the mean value of secondary flowers or fruits in treatment B (CB – SB; see Fig. 2 and Table 1). This total variation was 1.8 mm in limb length (Fig. 5A), 9.1 ovules (Fig. 5B), a fruit set of 0.1 (Fig. 5C), and a seed/ovule ratio of 14% (Fig. 5D). The comparisons between CB and SB distributions were statistically significant in all traits analyzed: limb length (t = 10.87, df = 134, P < 0.001), ovule number (t = 7.099, df = 117, P < 0.001), fruit set (not assuming homogeneity of variances: t = 3.515, df = 91, P < 0.01), and seed/ovule ratio (not assuming homogeneity of variances: t = 5.143, df = 95.743, P < 0.001).
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As in floral traits, most of the variation in fruit set and seed/ovule ratio was attributable to architectural effects, measured as the difference between CB (because flowers were removed from this position in the other treatments) and SA. This variation was 0.1 for fruit set (Fig. 5C) and was statistically significant (not assuming homogeneity of variances: t = 5.204, df = 146, P < 0.001). The variation in seed/ovule ratio resulting from architectural effects was 14.4%, and differences were statistically significant (not assuming homogeneity of variances: t = 5.7, df = 148.87, P < 0.001).
The variation attributable to resource competition with developing fruits was calculated by comparing secondary flowers in no competing fruit treatments (A and C) and secondary flowers/fruit in treatment B. In the case of limb length (Fig. 5A), no significant differences were found (t = –0.614, df = 275, P = 0.54), so no fruit set effects could be detected. For the number of ovules, differences were statistically significant (t = –3.953, df = 229, P < 0.001), but contrary to expectations, more ovules were found in the secondary flowers of treatment B (Fig. 5B).
On the other hand, no significant differences were found for fruit set (not assuming homogeneity of variances: t = –1.807, df = 269.239, P = 0.072) or seed/ovule ratio (t = –0.471, df = 180.43, P = 0.639) between secondary fruits in treatment A and secondary fruits in treatment B (Figs. 5C, D). Therefore, no effect attributable to competition with developing fruits was detected in fruit set and seed/ovule ratio.
DISCUSSION
This study shows a general pattern of within-inflorescence reduction in floral traits (petal size and ovule number) and female reproductive success (fruit set and seed/ovule ratio). This pattern of intrainflorescence variation was previously shown for S. acutifolia and was consistent among populations and years of study (Buide, 2004), although the causes of variation had not been disentangled. This within-inflorescence decline in different floral, fruit, and seed traits is a common pattern in plants often attributed to resource allocation (see Diggle, 2003 for a detailed review on the subject). An example of acropetal decline in ovule number over inflorescence was found by Thomson (1989) in 15 liliaceous species, even in those with basipetal floral anthesis. However, Thomson (1985) also found an increase in mean ovule number with time in Diervilla lonicera and explained it as a strategy for pollinator attraction specialization in first flowers, enabling them to invest in only a few ovules. In addition, Knight et al. (2005) suggested that high ovule numbers may be a bet-hedging strategy that allows plants to tolerate intraplant stochastic pollen receipt.
The removal of central (basal) and primary (lateral) flowers increased neither limb length nor the number of ovules in secondary (lateral) flowers, compared with flowers at the same position in inflorescences that were supplementary pollinated and produced fruits. The reduction in floral traits in this plant is therefore intrinsic to the inflorescence, and a reallocation of resources does not seem possible. Similarly, the decline in flower size found in Hydrophyllum appendiculatum (Wolfe, 1992) did not change when the resources to the inflorescences were manipulated and was considered a physical limitation of plant architecture. In the same way, Ashman and Hitchens (2000) found only an architectural effect without any distribution of resources for petal length in Fragaria virginiana. One of the reasons for this architectural effect may be that the flower peduncle diameter decreases from the central flowers to later lateral positions through the dichasium (M. L. Buide, personal observation, see also Fig. 1). In S. acutifolia, this variation in floral size may have ecological implications because this plant attracts differently sized pollinators, which range from bigger bees (Bombus spp.) to smaller bee-flies from the genus Bombylius (Buide, 2006). This diversification in pollinators could reflect a differential attraction for differently sized flowers within the same plant.
In the current study, there was pollen limitation in both fruit and seed/ovule ratio. In fruit set, pollen limitation did not take place in central (basal) flowers and was higher in the flowers that developed later in the inflorescence. This pollen limitation in later flowers may be due to a lower number of flowers in the male phase in the population when secondary lateral flowers are in the female phase. This higher pollen limitation in secondary flowers is consistent with the models for hermaphrodite plants with protandry developed by Brunet and Charlesworth (1995), who demonstrated that the reproductive success of first-position flowers is expected to be greater through female (relative to male) function, whereas the reverse pattern is expected in later-opening flowers. On the other hand, the reduction in fruit set and seed/ovule ratio from first to later flowers within the inflorescence is maintained when pollen is added to the flowers, so pollen limitations are only partly responsible.
When pollen limitation was excluded, architectural effects were responsible for most of the variation in fruit set and seed/ovule ratio. In that case, within-inflorescence decline seems independent of resource variation because no increase in reproductive success in secondary flowers was found when central and primary flowers are eliminated. Nicholls (1987) found architectural constraints in seed set in the inflorescence of Echium vulgare. However, the author did not separate the effect of resources within the inflorescence that may be reallocated from those mechanical limitations of vasculature imposed by inflorescence design, considering resource limitation as a type of architectural constraint. In contrast, Diggle (1995) and other authors (see also Ashman et al., 2001) separate the effect of resource redistribution in response to the failure of first fruits to develop from the variation inherent in the floral axis that cannot change in response to more resources. A number of studies among unrelated species provide support for these architectural effects. In Linaria canadensis, Wolfe and Denton (2001) demonstrated no effect of competition with developing fruits on fruit size, which was correlated with the thickness of the stem. In contrast, in Pancratium maritimum, the removal of the first developing flowers increased the number of fruit and the seed/ovule ratio of the remaining flowers (Medrano et al., 2000), attributing the reduction to competition for resources within the inflorescence. Pritchard and Edwards (2005) found that the addition of nutrients to the whole plant did not increase the fruit set of Crotalaria spectabilis, but removing developing fruits within the inflorescence increased the production of later fruits.
The variation in floral and fruit traits in response to resource competition can be considered as an example of phenotypic plasticity. One interesting observation is that levels of plasticity may change depending on the position within the inflorescence; proximal flowers may respond differently than the distal to resources. These differences in plasticity have been observed especially in gender allocation and was related to the evolution of mating systems, such as andromonoecy (Miller and Diggle, 2003). Similarly, different levels of plasticity have been found depending on plant size. For example, in F. virginiana, Ashman et al. (2001) found that unlike primary flowers, distal flowers do not increase ovule numbers with an increase in plant size. On the other hand, position effects in floral sex allocation independent of resources have been found in Clarkia unguiculata (Mazer and Dawson, 2001) and attributed to architectural or developmental changes associated with floral position and the differential movement or production of hormones throughout an inflorescence or flowering branch.
In contrast, this study suggests that the dichasial cymes of S. acutifolia have intrinsic constraints that limit plastic responses. Furthermore, in S. acutifolia, these limitations to plasticity may be partly overcome by a high variation in the number of floral branches produced by each individual plant. Up to 47 inflorescences were found in one marked individual in this species (M. L. Buide, personal observation), and interpopulation differences were previously found, with 50% of marked plants in one population having less than 12 inflorescences, while 50% of marked plants in the other population had less than six inflorescences (Buide, 2004). The next step should be the inclusion of inflorescences as a new level of study to measure where most of the variation is located and to determine how external resources affect the plant, which was not controlled in the current experiment. The opposite was found by Preston (1999), who found that plasticity at the level of the inflorescence compensated for fewer inflorescences by increasing the number of flowers and seeds produced per inflorescence.
In conclusion, this study clearly demonstrates that architectural effects are more important than resource competition in explaining intrainflorescence variation in floral traits and female reproductive success of S. acutifolia. On the other hand, a deficit of pollen was also found, especially in later flowers, which may reflect less pollen availability for secondary (lateral) flowers in the female phase in sequential blooming plants with protandry at the flower level.
FOOTNOTES
1 The author thanks J. A. Andrés and P. Gómez for assistance with fieldwork. M.L.B. was supported during this work by a postdoctoral fellowship from the University of Santiago de Compostela. Two anonymous reviewers provided many valuable comments that greatly improved the manuscript. 
2 Author for correspondence (e-mail: mlbuirea{at}upo.es)
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