Conclusion

To test the evolutionary significance and the function of the staminal lever in Salvia species, we quantitatively analyzed the "force-barrier-hypothesis" [21,26] using a biomechanical approach. This hypothesis states that the interspecific variation in the forces needed to release the lever in Salvia are the main reason for interspecific differences in the pollinator spectra. A Salvia population that undergoes an evolutionary change in these forces should therefore either specialize on a smaller number of strong flower visitors or generalize on a wider range of visitors that include weak ones. Small changes in joint anatomy could therefore lead to great differences in pollinator spectra and in populations of a Salvia species, which differ largely in specialization on pollinators. Because they have different pollinators, these populations might even become genetically isolated and be a starting point of speciation.

This interesting idea is not supported by the data presented in this paper. Despite the expected interspecific variability among Salvia species in the forces necessary to trigger the lever, these forces are generally low compared with the forces bees can exert. In two Salvia species specialized on bumblebees or carpenter bees and not visited by the honeybee, honeybees were, in contrast to the predictions of this hypothesis, strong enough to trigger the levers. Instead of the force required to trigger the lever, it is the flower-tube length that seems to exclude honeybees from the nectar of these two species. Nonetheless, the relative importance of the flower-tube length or the lever forces for specialization and speciation in Salvia cannot be finally evaluated because until now only 2% of all Salvia species have been investigated. In a large number of sages, the lever does not close the flower entrance and can therefore be circumvented easily (e.g., S. glutinosa). Furthermore, in species with a more derived flower morphology in which the lever closes the flower entrance (e.g., S. sclarea), the forces that have to be exerted while triggering the lever are low.

Therefore, we propose that these forces are of minor importance for pollinator shifts and specialization in the genus Salvia. We propose that the length of the flower tube in Salvia has the same role as in many other plant groups with tubular flowers or nectar spurs. Flower-tube length restricts access to nectar and is an important factor in recruiting a certain set of flower visitors.

With respect to the evolution of the staminal levers found in Salvia, we favor two possible functions involved in pollen transfer that are not mutually exclusive.

1. Pollen dispensing. Portioning of pollen by dispensing multiple small portions of pollen on successive visitors is found in many other plant species as an important mechanism for maximizing male fitness [42-44]. The hypothesis that staminal levers in Salvia may be involved in pollen dispensing is supported by the finding that the staminal levers can be released many times (more than 20 times in all tested sage species), resulting in (nearly) exactly the same force-distance curve with each release [21].

2. Exact pollen placement on the pollinator body. Exact pollen placement may be important for the reproductive success of plants for three reasons.

a. In subsequent visits of flowers of the same Salvia species, pollen placement at exactly the site where the style touches the insect enhances reproductive success by increasing the probability of pollen transfer [10,21].

b. In subsequent visits of an insect to different Salvia species, exact pollen placement on the pollinator's body as achieved by the staminal lever could avoid interspecific pollen transfer and thereby hybridization. This design would allow sympatric Salvia species to share a large number of pollinating species [20,45].

c. Exact, nototribic pollen placement as performed by the staminal lever in most Salvia species is thought to reduce pollen losses through grooming because bees seem to groom less effectively on their dorsal rather than on their lateral sides [46]. Nototribic pollen placement, in adddition to the fact that the thecae (and hence the pollen) in most bee-pollinated Salvia species are hidden in the upper lip of the flower during a bee's approach, should additionally reduce the influence of a flower visitor on its pollen uptake [47].

The previously mentioned possible functions of the staminal lever, i.e., optimizing pollen dispension and exact pollen placement, could allow Salvia species to specialize on certain bees as pollinators, which are known as "high-removal low-deposition" pollinators in the sense of Thomson et al. [48]. Therefore, the staminal lever of Salvia can be included in a list of floral features that optimize male reproductive success by controlling pollen release and pollen placement in bee-pollinated plants and that include buzz pollination, and the piston and brush mechanisms [9,10,14,49]. The immense species richness of the genus Salvia and the high morphological and functional diversity of its levers can then be interpreted as a by-product of selection on male reproductive success in a variable pollinator environment.

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