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Plant–animal interactions have important effects on community structure, population dynamics and trait evolution in plants. Pollen availability often limits seed production (Burd, 1994; Ashman et al., 2004) and also has consequences for the evolution of traits contributing to floral display (Kingsolver et al., 2001; Fenster et al., 2004). For traits associated with pollinator attraction, selection should often be affected by the level of pollen limitation (Ashman & Morgan, 2004). Spatio-temporal variation in pollen limitation has been demonstrated in several study systems (Campbell, 1987; Dieringer, 1992; Ågren, 1996; Alexandersson & Ågren, 1996; Dudash & Fenster, 1997; Baker et al., 2000; Goodwillie, 2001; Price et al., 2005), and may result in spatio-temporal variation in the average performance and population dynamics of plants. Spatio-temporal variation in interactions with pollinators may also influence trait-fitness relationships and translate into spatio-temporal variation in selection. While spatial variation in plant–pollinator interactions could promote divergent evolution of floral characters, temporal variation in interactions would limit the potential for divergent evolution (Caruso et al., 2003). This stresses the need for multipopulation studies over several years, as a single-year multipopulation study may emphasize the potential for divergent evolution, whereas a single-population multiyear study may emphasize the opposite. Spatio-temporal variation in selection on floral traits has sometimes been reported (Schemske & Horvitz, 1989; Caruso, 2000; Maad, 2000), but the causes of this variation have rarely been demonstrated experimentally (Fenster et al., 2004; but cf. Miller, 1981).
Prostrate growth is generally considered to be beneficial in grazed habitats (Lavorel et al., 1997), and many herbs in seminatural grasslands have a prostrate leaf rosette, a prostrate inflorescence, or both. Whether prostrate growth is also an evolutionary adaptation to grazing is less well documented (Kotanen & Bergelson, 2000). However, grazing is not the only biotic interaction that may affect reproductive success in relation to inflorescence height or ‘prostratedness’. Plant height may also affect attractiveness to pollinators (Peakall & Handel, 1993; Verbeek & Boasson, 1995; O’Connell & Johnston, 1998; Totland, 2001) and seed predators (Sauer & Feir, 1973; Hainsworth et al., 1984; Traveset, 1995).
Primula farinosa is a small perennial herb with a basal leaf rosette. It usually has a long-scaped inflorescence. However, in seminatural grasslands on the large island of Öland, south-east Sweden, populations are polymorphic for scape length and also include a short-scaped morph (Fig. 1). As a result, plants have their inflorescence displayed either well above the soil surface, or very close to the ground. This difference in scape morph may influence interactions with grazers, pollinators and seed predators, and variation in the intensity of these interactions may affect the relative performance of the two scape morphs.
Figure 1. Scape morphs of Primula farinosa. The common long-scaped morph (right) has a 2–20-cm-long scape. The short-scaped morph (left) has a markedly thicker and striate, 0–3-cm-long scape, and longer pedicels. It occurs on the island of Öland, Sweden.
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Severed scapes and fruit capsules with exit holes are readily linked to grazing or seed predation, respectively, and the magnitudes of these interactions are therefore straightforward to monitor. However, to infer pollination success from patterns of fruit initiation requires an experimental approach, as low levels of fruit initiation can also be attributed to a lack of resources. In a previous study of a single P. farinosa population on Öland, the short-scaped morph was more pollen-limited than the long-scaped morph, and the difference was larger in high than in low vegetation (Ehrlén et al., 2002). However, it is not known how far variation in pollination intensity affects among-population variation in fruit and seed initiation in the two scape morphs. To assess spatio-temporal variation in selection exerted by pollinators on scape length, it is necessary to link pollen limitation with scape length in multiple populations over several years.
We conducted a supplementary hand-pollination experiment in four populations in 2 yr to determine the extent to which variation in fruit and seed initiation can be attributed to interactions with pollinators. We asked: (1) Are fruit and seed initiation more strongly pollen-limited in the short-scaped than in the long-scaped morph? (2) Does pollen limitation vary between populations and years? (3) If present, does such spatio-temporal variation in pollen limitation translate into spatio-temporal variation in pollinator-mediated selection, or is the short-scaped morph consistently more pollen limited?
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This study has documented considerable spatio-temporal variation in pollen limitation, and has shown that fruit initiation is overall more strongly pollen-limited in the short-scaped than in the long-scaped morph of P. farinosa. However, the relative pollen limitation of long- and short-scaped plants did not vary across years or populations. Seed initiation was lower in the short-scaped than in the long scaped morph, and seed initiation increased after supplementary hand-pollination. However, the effect of hand-pollination on seed initiation did not differ between scape morphs. Morph-specific differences in pollen limitation were thus expressed mainly in terms of differences in fruit initiation. Several other studies have also shown that pollen limitation is a more important factor for fruit initiation than for seed initiation (reviewed by Burd, 1994).
We have demonstrated significant variation in pollen limitation, both among populations and between years. Pollen limitation of fruit initiation (1 − control/supplementary) in our four populations varied from −12 to 5% in 2001, and from −4 to 18% in 2002. These results emphasize the importance of conducting pollen-limitation experiments in several populations over several years to characterize the pollination regime for a given species (Campbell, 1987; Dieringer, 1992; Ågren, 1996; Alexandersson & Ågren, 1996; Dudash & Fenster, 1997; Baker et al., 2000; Goodwillie, 2001; Price et al., 2005).
Despite considerable spatio-temporal variation in pollen limitation, we did not detect any significant variation in pollinator-mediated selection on scape morph. This is surprising, especially given that we did find among-population variations in the relative fruit initiation between morphs. Apparently the link between spatio-temporal variations in selection in a pollen-limited plant and spatio-temporal variations in pollinator-mediated selection is not straightforward.
The long-scaped morph was, overall, less pollen-limited than the short-scaped morph. The most plausible explanation for this is that the pollinators of P. farinosa use visual cues to find their flowers, and that the long-scaped inflorescences are detected more easily (Omura & Honda, 2005). In addition, insect pollinators, including bees, butterflies and syrphids, may adjust their behaviour to avoid predators when foraging (Dukas, 2001; Munoz & Arroyo, 2004). Pollinators may avoid the short-scaped morph if landing close to the ground increases the predation risk. Plant height also affects plant fitness through attractiveness to pollinators in other plant species (Peakall & Handel, 1993; Verbeek & Boasson, 1995; O’Connell & Johnston, 1998; Totland, 2001). However, plant height is usually strongly affected by environmental factors and plant age, and the evolutionary outcome of this phenotypic selection may be weak. In P. farinosa, phenotypic selection on scape morph is likely to correspond well with genetic selection, as our crossing experiments suggest a strong heritability.
Pollen limitation did not explain all the difference in fruit initiation between the two scape morphs. The long-scaped morph also outperformed the short-scaped morph after supplementary hand-pollination. This could reflect morph-specific differences in resources available for fruit maturation. The developing fruits on short-scaped plants are likely to be more shaded by surrounding vegetation and may therefore have a lower photosynthetic capacity than fruits on long-scaped plants. The leaf rosette of the short-scaped morph might also be shaded by its own infructescence. Alternatively, resource division between fruit development and other functions may differ inherently between the two scape morphs. These nonpollinator-related factors could be responsible for the spatial variation in relative fruit initiation between the morphs, a pattern that pollen limitation did not explain.
Seed mass was negatively related to the proportion of ovules initiating seed development. Baker et al. (1994) have shown that larger P. farinosa seeds germinate better and more quickly, and produce larger seedlings. Plants with a low seed set may thus produce seedlings with a competitive advantage, which could compensate for the low seed number. However, despite a 12% lower seed initiation, the short-scaped morph did not produce larger seeds than the long-scaped morph.
Pollen limitation is likely to vary in space and time in many plant species. As demonstrated by the present study, such variation is not necessarily associated with variation in selection on floral characters. Additional experimental studies exploring the relationship between pollen limitation and selection on floral traits are clearly needed. Nevertheless, this study has established that fruit set is, overall, more strongly pollen-limited in the short-scaped than in the long-scaped morph of P. farinosa. Interactions with pollinators are thus likely to be important for the relative fecundity of the two scape morphs and the maintenance of this striking polymorphism. A full understanding of the dynamics of this polymorphism will require the incorporation of spatio-temporal variation in interactions with other biotic agents that are likely to affect selection on scape length, such as seed predators and grazers. With the present study in mind, the link between spatio-temporal variation in, for example, grazing intensity and spatio-temporal variation in grazing-mediated selection for prostratedness would also require attention.